Physical evidence of predatory behavior in Tyrannosaurus rex

Feeding strategies of the large theropod, Tyrannosaurus rex, either as a predator or a scavenger, have been a topic of debate previously compromised by lack of definitive physical evidence. Tooth drag and bone puncture marks have been documented on suggested prey items, but are often difficult to attribute to a specific theropod. Further, postmortem damage cannot be distinguished from intravital occurrences, unless evidence of healing is present. Here we report definitive evidence of predation by T. rex: a tooth crown embedded in a hadrosaurid caudal centrum, surrounded by healed bone growth. This indicates that the prey escaped and lived for some time after the injury, providing direct evidence of predatory behavior by T. rex. The two traumatically fused hadrosaur vertebrae partially enclosing a T. rex tooth were discovered in the Hell Creek Formation of South Dakota.One of the most daunting tasks of paleontology is inferring the behavior and feeding habits of extinct organisms. Accurate reconstruction of the lifestyle of extinct animals is dependent on the fossil evidence and its interpretation is most confidently predicated on analogy with modern counterparts (1–6). This challenge to understanding the lifestyle of extinct animals is exemplified by the controversy over the feeding behavior of the Late Cretaceous theropod Tyrannosaurus rex (3, 7–17). Although predation and scavenging have often been suggested as distinct feeding behavior alternatives (3, 7–9, 11–17), these terms merit semantic clarification. In this study, predation is considered a subset of feeding behavior, by which any species kills what it eats. Although the term “predator” is used to distinguish such animals from obligate scavengers, it does not imply that the animal did not also scavenge.Ancient diets can be readily reconstructed on the basis of the available evidence, although their derivation (e.g., predation or scavenging behavior) often remains elusive. Speculation as to dinosaur predation has ranged from inferences based on skeletal morphology, ichnofossils such as bite marks, coprolites, stomach contents, and trackways and, by more rarely, direct predator–prey skeletal associations (3, 4, 18–23).Direct evidence of predation in nonavian dinosaurs other than tyrannosaurids has been observed in rare instances, such as the Deinonychus–Tenontosaurus kill site of the Cloverly Formation where the remains of both were found in close association along with shed teeth (9, 24), and the “fighting dinosaurs” from the Gobi Desert, in which a Velociraptor and Protoceratops were found locked in mortal combat (9, 17). The evidence on tyrannosaurids is more limited. Putative stomach contents, such as partially digested juvenile hadrosaur bones, have been reported in association with tyrannosaurid remains (3, 12, 18). This latter instance only represents physical evidence of the last items consumed before the animal’s death, an indicator of diet but not behavior.Mass death assemblages of ornithischians frequently preserve shed theropod teeth (6, 22, 24). Lockley et al. (23) suggest such shed teeth are evidence of scavenging behavior. It is widely argued that T. rex procured food through obligate scavenging rather than hunting (11, 14, 25–27) despite the fact that there is currently no modern analog for such a large bodied obligate scavenger (26). Horner (25) argued that T. rex was too slow to pursue and capture prey items (14) and that large theropods procured food solely through scavenging, rather than hunting (11, 25). Horner also suggested that the enlarged olfactory lobes in T.rex were characteristic of scavengers (25). More recent studies (28, 29) determined the olfactory lobes of modern birds are “poorly developed,” inferring that enlarged olfactory lobes in T. rex are actually a secondary adaptation for predation navigation “to track mobile, dispersed prey” (30). T. rex has a calculated bite force stronger than that of any other terrestrial predator (7), between 35,000 and 57,000 Newtons (30, 31), and possible ambulatory speeds between 20 and 40 kph (7, 15, 16), documenting that it had the capability to pursue and kill prey items.Healed injuries on potential prey animals provide the most unequivocal evidence of survival of a traumatic event (e.g., predation attempt) (3, 32, 33), and several reports attribute such damage to T. rex (4, 17, 19, 20). These include broken and healed proximal caudal vertebral dorsal spines in Edmontosaurus (17) and healed cranial lesions in Triceratops (4, 19). Although the presence of healed injuries demonstrates that an animal lived long enough after the attack to create new bone at the site of the damage (a rare occurrence in the fossil record) (19), the healing usually obliterates any clear signature linking the injury to a specific predator. Bite traces (e.g., raking tooth marks on bone and puncture wounds in the bones of possible prey animals) attributed to T. rex (2, 4, 19) are ambiguous, because the damage inflicted upon an animal during and after a successful hunt mirrors feeding during scavenging. This makes distinction between the two modes of food acquisition virtually impossible with such evidence (3, 34–38).Tooth marks, reported from dinosaur bone-bearing strata worldwide (e.g., 2–4, 8, 19, 20, 39, 40), are further direct evidence of theropod feeding behavior, attributed by some to specific theropod groups (2, 4, 19, 20). Happ (19) and Carpenter (17) identified theropods to family and genus by matching spaces to parallel marks (traces) with intertooth distance. Happ (19) described opposing conical depressions on a left supraorbital Triceratops horn that was missing its distal third (tip), attributing them to a bite by either a T. rex or a crocodilian. Happ (19) stated that the spacing of the parallel marks present on the left squamosal of the same individual matched the intertooth distance of tyrannosaurids. The presence of periosteal reaction documents healing. This contrasts with the report by Farlow and Holtz (3) and again by Hone and Rauhut (20) of the same Hypacrosaurus fibula containing a superficially embedded theropod tooth. Absence of bone reaction precludes confident attribution to predation.Two coalesced hadrosaur (compare with Edmontosaurus annectens) caudal vertebrae were discovered in the Hell Creek Formation of Harding County, South Dakota (40). Archosaur fauna identified in this site include crocodiles, dinosaurs, and birds (41). Physical evidence of dental penetration and extensive infection (osteomylitis) of the fused vertebral centra and healing (bone overgrowth) document an unsuccessful attack by a large predator. A tooth crown was discovered within the wound, permitting identification of the predator as T. rex. This is unambiguous evidence that T. rex was an active predator, fulfilling the criteria that Farlow and Holtz (3) advanced. As T. rex comprises between 1% and 16% of the Upper Cretaceous dinosaurian fauna in Western North America (41–45), its status as a predator or obligate scavenger is nontrivial and could have significant implications for paleoecological reconstructions of that time period. The present contribution provides unique information demonstrating the ecological role for T. rex as that of an active predator. Despite this documentation of predatory behavior by T. rex, we do not make the argument that T. rex was an obligate predator. Like most modern large predators (27, 45) it almost certainly did also scavenge carcasses (9, 16).     

From the Cover: Canine sexual dimorphism in Ardipithecus ramidus was nearly human-like

Body and canine size dimorphism in fossils inform sociobehavioral hypotheses on human evolution and have been of interest since Darwin’s famous reflections on the subject. Here, we assemble a large dataset of fossil canines of the human clade, including all available Ardipithecus ramidus fossils recovered from the Middle Awash and Gona research areas in Ethiopia, and systematically examine canine dimorphism through evolutionary time. In particular, we apply a Bayesian probabilistic method that reduces bias when estimating weak and moderate levels of dimorphism. Our results show that Ar. ramidus canine dimorphism was significantly weaker than in the bonobo, the least dimorphic and behaviorally least aggressive among extant great apes. Average male-to-female size ratios of the canine in Ar. ramidus are estimated as 1.06 and 1.13 in the upper and lower canines, respectively, within modern human population ranges of variation. The slightly greater magnitude of canine size dimorphism in the lower than in the upper canines of Ar. ramidus appears to be shared with early Australopithecus, suggesting that male canine reduction was initially more advanced in the behaviorally important upper canine. The available fossil evidence suggests a drastic size reduction of the male canine prior to Ar. ramidus and the earliest known members of the human clade, with little change in canine dimorphism levels thereafter. This evolutionary pattern indicates a profound behavioral shift associated with comparatively weak levels of male aggression early in human evolution, a pattern that was subsequently shared by Australopithecus and Homo.

A small canine tooth with little sexual dimorphism is a well-known hallmark of the human condition. The small and relatively nonprojecting deciduous canine of the first known fossil of Australopithecus, the Taung child skull, was a key feature used by Raymond Dart for his inference that the fossil represented an early stage of human evolution (1). However, recovery of additional Australopithecus fossils led to the canine of Australopithecus africanus to be characterized as large (compared to that of humans or “robust australopithecines”) and its morphology primitive, based on a projecting main cusp and crown structures lacking or hardly expressed in Homo (2). Later, the perception of a large and primitive canine was enhanced by the discovery and recognition of Australopithecus afarensis and Australopithecus anamensis (3–8), the latter species extending back in time to 4.2 million years ago (Ma). Although assessments of canine size variation and sexual dimorphism in Au. afarensis were hampered by limited sample sizes (9, 10), some suggested that the species had a more dimorphic canine than do humans, equivalent in degree to the bonobo (11) or to chimpanzees and orangutans (12). Initially, Au. anamensis was suggested to express greater canine dimorphism than did Au. afarensis (13, 14). However, based on a somewhat larger sample size, this is now considered to be the case with the tooth root but not necessarily its crown (15–17).Throughout the 1990s and 2000s, a pre-Australopithecus record of fossils spanning >6.0 to 4.4 Ma revealed that the canines of these earlier forms did not necessarily exceed those of Au. afarensis or Au. anamensis in general size (18–28). However, all these taxa apparently possessed canine crowns on average about 30% larger than in modern humans, which makes moderately high levels of sexual dimorphism potentially possible. Canine sexual dimorphism, combined with features such as body size dimorphism, inform sociobehavioral and ecological adaptations of past and present primates, and therefore have been of considerable interest since Darwin’s 1871 considerations (29–57). In particular, the relationship of canine size dimorphism (and/or male and female relative canine sizes) with reproductive strategies and aggression/competition levels in primate species have been a continued focus of interest (14, 33, 35–45, 49–56). Conspecific-directed agonistic behavior in primates related to mate and/or resource competition can be particularly intense among males both within and between groups (14, 44, 57). It is widely recognized that a large canine functions as a weapon in intra- and intergroup incidences of occasional lethal aggression (45, 58–61), and a large, tall canine has been shown or inferred to significantly enhance male fitness (50, 56). Hence, canine size and dimorphism levels in fossil species provide otherwise unavailable insights into their adaptive strategies.Here, we apply a recently developed method of estimating sexual size dimorphism from fossil assemblages of unknown sex compositions, the posterior density peak (pdPeak) method (62), and reexamine canine sexual dimorphism in Ardipithecus ramidus at ∼4.5 Ma. We include newly available fossils recovered from the Middle Awash and Gona paleoanthropological research areas in the Afar Rift, Ethiopia (26, 63, 64) in order to obtain the most reliable dimorphism estimates currently possible. We apply the same method to Australopithecus, Homo, and selected fossil apes, and evaluate canine sexual dimorphism through evolutionary time.We operationally define canine sexual dimorphism as the ratio between male and female means of basal canine crown diameters (the m/f ratio). Because the canines of Ar. ramidus, Au. anamensis, and extant and fossil apes are variably asymmetric in crown shape, we examine the maximum basal dimension of the crown. This can be either the mesiodistal crown diameter or a maximum diameter taken from the distolingual to mesiobuccal crown base (7, 27, 65). In the chronologically later Au. afarensis and all other species of Australopithecus sensu lato and Homo, we examine the more widely available conventional metric of buccolingual breadth, which corresponds to or approximates the maximum basal crown diameter. In anthropoid primates, canine height is more informative than basal canine diameter as a functional indicator of aggression and/or related display (14, 41–44). We therefore also examine available unworn and minimally worn fossil canines with reliable crown heights.     

Coulomb interaction,phonons, and superconductivity in twisted bilayer graphene

The polarizability of twisted bilayer graphene, due to the combined effect of electron–hole pairs, plasmons, and acoustic phonons, is analyzed. The screened Coulomb interaction allows for the formation of Cooper pairs and superconductivity in a significant range of twist angles and fillings. The tendency toward superconductivity is enhanced by the coupling between longitudinal phonons and electron–hole pairs. Scattering processes involving large momentum transfers, Umklapp processes, play a crucial role in the formation of Cooper pairs. The magnitude of the superconducting gap changes among the different pockets of the Fermi surface.

Twisted bilayer graphene (TBG) shows a complex phase diagram which combines superconducting and insulating phases (1, 2) and resembles strongly correlated materials previously encountered in condensed matter physics (3–6). On the other hand, superconductivity seems more prevalent in TBG (7–11), while in other strongly correlated materials magnetic phases are dominant.The pairing interaction responsible for superconductivity in TBG has been intensively studied. Among other possible pairing mechanisms, the effect of phonons (12–19) (see also ref. 20), the proximity of the chemical potential to a van Hove singularity in the density of states (DOS) (21–25) and excitations of insulating phases (26–28) (see also refs. 29–31), and the role of electronic screening (32–35) have been considered.In the following, we analyze how the screened Coulomb interaction induces pairing in TBG. The calculation is based on the Kohn–Luttinger formalism (36) for the study of anisotropic superconductivity via repulsive interactions. The screening includes electron–hole pairs (37), plasmons (38), and phonons (note that acoustic phonons overlap with the electron–hole continuum in TBG). Our results show that the repulsive Coulomb interaction, screened by plasmons and electron–hole pairs only, leads to anisotropic superconductivity, although with critical temperatures of order T_c ∼ 10⁻³ to 10⁻² K. The inclusion of phonons in the screening function substantially enhances the critical temperature, to T_c ∼ 1 to 10 K.     

An integrative skeletal and paleogenomic analysis of stature variation suggests relatively reduced health for early European farmers

Human culture, biology, and health were shaped dramatically by the onset of agriculture ∼12,000 y B.P. This shift is hypothesized to have resulted in increased individual fitness and population growth as evidenced by archaeological and population genomic data alongside a decline in physiological health as inferred from skeletal remains. Here, we consider osteological and ancient DNA data from the same prehistoric individuals to study human stature variation as a proxy for health across a transition to agriculture. Specifically, we compared “predicted” genetic contributions to height from paleogenomic data and “achieved” adult osteological height estimated from long bone measurements for 167 individuals across Europe spanning the Upper Paleolithic to Iron Age (∼38,000 to 2,400 B.P.). We found that individuals from the Neolithic were shorter than expected (given their individual polygenic height scores) by an average of −3.82 cm relative to individuals from the Upper Paleolithic and Mesolithic (P = 0.040) and −2.21 cm shorter relative to post-Neolithic individuals (P = 0.068), with osteological vs. expected stature steadily increasing across the Copper (+1.95 cm relative to the Neolithic), Bronze (+2.70 cm), and Iron (+3.27 cm) Ages. These results were attenuated when we additionally accounted for genome-wide genetic ancestry variation: for example, with Neolithic individuals −2.82 cm shorter than expected on average relative to pre-Neolithic individuals (P = 0.120). We also incorporated observations of paleopathological indicators of nonspecific stress that can persist from childhood to adulthood in skeletal remains into our model. Overall, our work highlights the potential of integrating disparate datasets to explore proxies of health in prehistory.

The agricultural revolution—beginning ∼12,000 B.P. in the Fertile Crescent zone (1, 2) and then spreading (3–5) or occurring independently (6, 7) across much of the inhabited planet—precipitated profound changes to human subsistence, social systems, and health. Seemingly paradoxically, the agricultural transition may have presented conflicting biological benefits and costs for early farming communities (8, 9). Specifically, demographic reconstructions from archaeological and population genetic records suggest that the agricultural transition led to increased individual fitness and population growth (6, 10–12), likely due in part to new food production and storage capabilities. Yet, bioarchaeological analyses of human skeletal remains from this cultural period suggest simultaneous declines in individual physiological well-being and health, putatively from 1) nutritional deficiency and/or 2) increased pathogen loads as a function of greater human population densities, sedentary lifestyles, and proximity to livestock (9, 13–18).To date, anthropologists have used two principal approaches to study health across the foraging-to-farming transition in diverse global regions (13, 19, 20). The first approach involves identifying paleopathological indicators of childhood stress that persist into adult skeletal remains. For example, porotic hyperostosis (porous lesions on the cranial vault) and cribra orbitalia (porosity on the orbital roof) reflect a history of bone marrow hypertrophy or hyperplasia resulting from one or more periods of infection, metabolic deficiencies, malnutrition, and/or chronic disease (21–26). Meanwhile, linear enamel hypoplasia (transverse areas of reduced enamel thickness on teeth) occurs in response to similar childhood physiological stressors (e.g., disease, metabolic deficiencies, malnutrition, weaning) that disrupt enamel formation in the developing permanent dentition (27–30). Broadly, these paleopathological indicators of childhood stress tend to be observed at higher rates among individuals from initial farming communities relative to earlier periods, potentially reflecting their overall “poorer” health (14, 31–36).A second approach uses skeleton-based estimates of achieved adult stature as a proxy for health during childhood growth and development (37–39). Since stature is responsive to the influences of nutrition and disease burden alongside other factors, relatively short “height-for-age” (or “stunting”) has been used as an indicator of poorer health in both living and bioarchaeological contexts (39–43). When studying the past, individual stature can be estimated from long bone measurements and regression equations (44–47). Using these methods, multiple prior studies have reported a general profile of relatively reduced stature for individuals from early agricultural societies in Europe (15, 48–50), North America (51–53), the Levant (16, 32), and Asia (54, 55). For example, estimated average adult mean statures for early farmers are ∼10 cm shorter relative to those for preceding hunter-gatherers in both western Europe (females, −8 cm; males, −14 cm) (49, 50) and the eastern Mediterranean (females, −11 cm; males, −8 cm) (56). This pattern is not universal, as a few studies do not report such changes (57, 58); the variation could be informative with respect to identifying potential underlying factors (59).However, in addition to environmental effects like childhood nutrition and disease, inherited genetic variation can have an outsized impact on terminal stature, with ∼80% of the considerable degree of height variation within many modern populations explainable by heritable genetic variation (60–63). Moreover, migration and gene flow likely accompanied many subsistence shifts in human prehistory. For example, there is now substantial paleogenomic evidence of extensive population turnover across prehistoric Europe (64–69). Therefore, from osteological studies alone, we are unable to quantify the extent to which temporal changes in height reflect variation in childhood health vs. changes/differences in the frequencies of alleles associated with height variation.In this study, we have performed a combined analysis of ancient human paleogenomic and osteological data where both are available from the same n = 167 prehistoric European individuals representing cultural periods from the Upper Paleolithic (∼38,000 B.P.) to the Iron Age (∼2,400 B.P.). This approach allows us to explore whether “health,” as inferred from the per-individual difference between predicted genetic contributions to height and osteological estimates of achieved adult height, changed over the Neolithic cultural shift to agriculture in Europe. When craniodental elements were preserved and available for analysis (n = 98 of the 167 individuals), we also collected porotic hyperostosis, cribra orbitalia, and linear enamel hypoplasia paleopathological data in order to examine whether patterns of variation between osteological height and genetic contributions to height are explained in part by the presence/absence of these indicators of childhood or childhood-inclusive stress.     

From the Cover: Predicting overfishing and extinction threats in multispecies fisheries

Threats to species from commercial fishing are rarely identified until species have suffered large population declines, by which time remedial actions can have severe economic consequences, such as closure of fisheries. Many of the species most threatened by fishing are caught in multispecies fisheries, which can remain profitable even as populations of some species collapse. Here we show for multispecies fisheries that the biological and socioeconomic conditions that would eventually cause species to be severely depleted or even driven extinct can be identified decades before those species experience high harvest rates or marked population declines. Because fishing effort imposes a common source of mortality on all species in a fishery, the long-term impact of a fishery on a species is predicted by measuring its loss rate relative to that of species that influence the fishery’s maximal effort. We tested our approach on eight Pacific tuna and billfish populations, four of which have been identified recently as in decline and threatened with overfishing. The severe depletion of all four populations could have been predicted in the 1950s, using our approach. Our results demonstrate that species threatened by human harvesting can be identified much earlier, providing time for adjustments in harvesting practices before consequences become severe and fishery closures or other socioeconomically disruptive interventions are required to protect species.Marine fisheries are an important global source of food and livelihoods (1–4), but there are concerns that current fishing practices threaten some marine species with severe depletion or eventual extinction (2–5). Many of the largest commercial fishing methods, such as trawling, longlining, and seining, unavoidably catch multiple species simultaneously (6–9). Multispecies fisheries pose a particular threat of extinction or severe depletion because fishing can remain profitable as long as some valuable species remain abundant, even while others collapse (6–11). In contrast, in a single-species fishery profits tend to fall as the target population declines, thereby removing the incentive to fish before extinction occurs (10). Multispecies fisheries pose a threat to two types of species or stocks (populations): (i) commercially valued species, called “weak stocks”, which are more vulnerable to overharvesting than are other commercially valuable species (6), and (ii) by-catch species, which are caught accidentally and create little economic incentive to cease fishing as their populations collapse because they have little or no commercial value (7–9).Failure to prevent collapse of weak stocks and by-catch species can impose substantial long-term environmental and economic costs. Slow-growing populations are most likely to collapse, but can take several decades to recover (5). Recovery often requires long-term fishery closures or reductions in effort, having substantial economic and social consequences (3, 5). Moreover, population declines caused by one fishery can diminish yields and profits in other commercial or artisanal fisheries that depend on the same species (e.g., ref. 12).Despite these costs, species threatened by fishing have rarely been identified until after their populations have declined substantially (2–5, 7, 8). Assessments of fishery impacts on species mostly focus on estimating current exploitation rates or past population trends (13–15), which identifies already declining species rather than predicting future declines. Data limitations have made empirical prediction of future threats from fishing challenging, particularly for weak stocks and by-catch species. Oceans are difficult to sample extensively, and few economic incentives exist to gather data on species other than the most commercially valued species (7, 8). Some predictive models (e.g., ref. 16) have been developed to forecast the impacts of some fisheries, but these are often data intensive. Some of the characteristics that make a population susceptible to overfishing are well known—for example, low population growth rates (3–11, 17, 18), high value and/or low fishing costs (10, 11, 17–19), and schooling behavior (18). Recently, some correlative approaches based on these characteristics have been developed for assessing likely relative threats to data-poor species (4, 20–22). However, predicting the severity of future threats in absolute terms with this type of approach can be challenging.Here, we present a mechanistic approach that uses readily available data to predict the potential of current fishing practices, if maintained, to eventually cause a population to be driven extinct or “overfished”, here defined as depletion below its maximum sustainable yield (MSY) abundance (N_MSY) (3). Our approach identifies combinations of biological and socioeconomic conditions that are likely to eventually lead to high mortality rates and population declines. As we show, these conditions can be identified long before either occurs.We test the predictive power of our approach on eight tuna and billfish populations of the Western and Central Pacific Ocean fisheries. High-seas tuna and billfish have elicited recent conservation concern due to significant population declines and range contractions found in many species (17, 23, 24). Three of the populations in our study, bigeye tuna (Thunnus obesus) and both the northern and the southern striped marlin (Tetrapturus audax) populations, have been recently identified as experiencing overfishing—meaning their exploitation rates have exceeded the MSY exploitation rate (F_MSY) (24–27). A fourth, blue marlin (Makaira nigricans), whose overfishing status has been subject to considerable uncertainty (28), has undergone a significant population decline and range contraction (13, 23, 28). We determine whether our approach could have predicted threats to these four populations, using data from as early as the 1950s, and assess the threats predicted by the latest available data to all populations.     

Volcanically driven lacustrine ecosystem changes during the Carnian Pluvial Episode (Late Triassic)

The Late Triassic Carnian Pluvial Episode (CPE) saw a dramatic increase in global humidity and temperature that has been linked to the large-scale volcanism of the Wrangellia large igneous province. The climatic changes coincide with a major biological turnover on land that included the ascent of the dinosaurs and the origin of modern conifers. However, linking the disparate cause and effects of the CPE has yet to be achieved because of the lack of a detailed terrestrial record of these events. Here, we present a multidisciplinary record of volcanism and environmental change from an expanded Carnian lake succession of the Jiyuan Basin, North China. New U–Pb zircon dating, high-resolution chemostratigraphy, and palynological and sedimentological data reveal that terrestrial conditions in the region were in remarkable lockstep with the large-scale volcanism. Using the sedimentary mercury record as a proxy for eruptions reveals four discrete episodes during the CPE interval (ca. 234.0 to 232.4 Ma). Each eruptive phase correlated with large, negative C isotope excursions and major climatic changes to more humid conditions (marked by increased importance of hygrophytic plants), lake expansion, and eutrophication. Our results show that large igneous province eruptions can occur in multiple, discrete pulses, rather than showing a simple acme-and-decline history, and demonstrate their powerful ability to alter the global C cycle, cause climate change, and drive macroevolution, at least in the Triassic.

The Carnian Pluvial Episode (CPE; ca. 234 to ∼232 Ma; Late Triassic) was an interval of significant changes in global climate and biotas (1, 2). It was characterized by warming (3, 4) and enhancement of the hydrological cycle (5–7), linked to repeated C isotope fluctuations (8–11) and accompanied by increased rainfall (1), intensified continental weathering (9, 12), shutdown of carbonate platforms (13), widespread marine anoxia (4), and substantial biological turnover (1, 2, 10). Available stratigraphic data indicate that the Carnian climatic changes broadly coincide with, and could have been driven by, the emplacement of the Wrangellia large igneous province (LIP) (2, 4, 7, 8, 10, 14, 15) (Fig. 1A). It is postulated that the voluminous emission of volcanic CO₂, with consequent global warming and enhancement of a mega-monsoonal climate, was responsible for the CPE (9, 16), although the link is imprecise (2, 17) because the interval of Wrangellian eruptions have not yet been traced in the sedimentary records encompassing the CPE.Open in a separate windowFig. 1.Location and geological context for the study area. (A) Paleogeographic reconstruction for the Carnian (∼237 to 227 Ma) Stage (Late Triassic), showing locations of the study area and volcanic centers (revised after ref. 4, with volcanic data from refs. 4, 7, 49, and 50). (B) Tectono-paleogeographic map of the NCP during the Late Triassic (modified from ref. 21), showing the location of the study area. (C) Stratigraphic framework of the Upper Chunshuyao Formation (CSY) to the Lower Yangshuzhuang (YSZ) Formation from the Jiyuan Basin (modified from ref. 20). Abbreviations: LIP, Large Igneous Province; QDOB, Qingling-Dabie Orogenic Belt; S-NCP, southern NCP; SCP, South China Plate; Fm., Formation; m & s, coal, mudstone, and silty mudstone; s., sandstone; c, conglomerate; Dep. env., Depositional environment; and C.-P., Coniopteris-Phoenicopsis.The CPE was originally identified because of changes in terrestrial sedimentation, but most subsequent studies have been on marine strata (2, 4, 7–10). By contrast, much less is known about the effects of this climatic episode on terrestrial environments (2), although there were major extinctions and radiations among animals (including dinosaurs, crocodiles, turtles, and the first mammals and insects) and modern conifer families (2). Some of the new organisms may have flourished because of the spread of humid environments, such as the turtles and metoposaurids (18, 19).In this study, we have investigated terrestrial sediments from the Zuanjing-1 (ZJ-1) borehole in the Jiyuan Basin of the southern North China Plate (NCP) and use zircon U–Pb ages from two tuffaceous claystone horizons, fossil plant biostratigraphy, and organic C isotope (δ¹³C_org) and Hg chemostratigraphy to identify the CPE and volcanic activity.     

Competing interactions give rise to two-state behavior and switch-like transitions in charge-rich intrinsically disordered proteins

The most commonly occurring intrinsically disordered proteins (IDPs) are polyampholytes, which are defined by the duality of low net charge per residue and high fractions of charged residues. Recent experiments have uncovered nuances regarding sequence–ensemble relationships of model polyampholytic IDPs. These include differences in conformational preferences for sequences with lysine vs. arginine and the suggestion that well-mixed sequences form a range of conformations, including globules, conformations with ensemble averages that are reminiscent of ideal chains, or self-avoiding walks. Here, we explain these observations by analyzing results from atomistic simulations. We find that polyampholytic IDPs generally sample two distinct stable states, namely, globules and self-avoiding walks. Globules are favored by electrostatic attractions between oppositely charged residues, whereas self-avoiding walks are favored by favorable free energies of hydration of charged residues. We find sequence-specific temperatures of bistability at which globules and self-avoiding walks can coexist. At these temperatures, ensemble averages over coexisting states give rise to statistics that resemble ideal chains without there being an actual counterbalancing of intrachain and chain-solvent interactions. At equivalent temperatures, arginine-rich sequences tilt the preference toward globular conformations whereas lysine-rich sequences tilt the preference toward self-avoiding walks. We also identify differences between aspartate- and glutamate-containing sequences, whereby the shorter aspartate side chain engenders preferences for metastable, necklace-like conformations. Finally, although segregation of oppositely charged residues within the linear sequence maintains the overall two-state behavior, compact states are highly favored by such systems.

Significant fractions of eukaryotic proteomes are made up of intrinsically disordered regions (IDRs) (1). Conformational heterogeneity (2) is a defining hallmark of IDRs (3–5). Studies over the past decade have helped quantify relationships (6) that connect sequence-encoded information within IDRs to properties of conformational ensembles such as overall sizes and shapes, the amplitudes of spontaneous conformational fluctuations, and the dynamics of interconverting between distinct conformational states (7–19). These sequence–ensemble relationships have direct functional consequences that have been uncovered via studies based on biophysical, biochemical, and engineering approaches (5, 20–38). Our work, which is focused on physical principles underlying sequence–ensemble relationships of IDRs, is of direct relevance to understanding how IDRs function.Charged residues are key determinants of sequence–ensemble relationships of IDRs (19, 39–41). They contribute through highly favorable free energies of hydration (42) and long-range electrostatic interactions. Net charge per residue (19, 39, 40) and the patterning of oppositely charged residues (43–45) are useful order parameters for describing sequence–ensemble relationships and interactions of charge-rich IDRs (46). Both features can be modulated through posttranslational modifications (47–51), charge renormalization by solution ions (52), and charge regulation through context- and conformation-dependent uptake and release of protons (53).Polyampholytes feature roughly equivalent numbers of oppositely charged residues, and they make up more than 70% of known IDRs (7, 17). For a given amino acid composition, which sets the fraction of charged residues and the net charge per residue, it has been shown that the linear mixing vs. segregation of oppositely charged residues can have a profound impact on sequence–ensemble relationships of polyampholytic IDRs (31, 32, 43). Specifically, for a given set of solution conditions, sequences featuring uniform linear distributions of oppositely charged residues are predicted to favor more expanded conformations compared to sequences with identical amino acid compositions where the oppositely charged residues are segregated into distinct blocks along the linear sequence. These predictions made using simulation and theory (43, 44, 54) have been confirmed using different experiments (31–33, 41, 55).The ensemble-averaged radii of gyration (R_g) of flexible polymers follow scaling relationships of the form R_g ∼ N^ν. Here, N denotes the number of residues and the scaling exponent ν is a measure of the length scale over which conformational fluctuations are correlated. For homopolymers or systems that are effective homopolymers, ν has four limiting values, viz., 0.33, 0.5, 0.59, or 1, corresponding to globules, Flory random coils (FRCs), self-avoiding walks, and rod-like conformations, respectively (56). Atomistic simulations performed at fixed temperatures suggest that ν ≈ 0.59 (43) for strong, well-mixed polyampholytes (17). The explanation for this behavior is as follows. Electrostatic attractions and repulsions are realized on similar length scales for well-mixed sequences. These interactions screen one another, and the highly favorable free energies of hydration become the main determinants of overall sizes and shapes of well-mixed strong polyampholytes (17). In contrast, compact conformations are formed by strong polyampholytes where oppositely charged residues are segregated into distinct blocks. Here, the electrostatic attractions between oppositely charged blocks can outcompete opposing effects of favorable solvation. These inferences were gleaned using sequences comprising 1:1 ratios of Lys and Glu (43). In the original simulations, the reference free energies of hydration of all charged residues were treated as being quantitatively equivalent and highly favorable. This leads to the hypothesis that Lys and Arg are interoperable with one another as determinants of sequence–ensemble relationships of IDRs (17). A similar inference emerges regarding the interoperability of Asp and Glu with respect to one another. The recent work of Sørensen and Kjaergaard has challenged these inferences (57). Using a system where model IDRs were deployed as flexible linkers between interaction domains, Sørensen and Kjaergaard used their measurements to estimate the relationships between amino acid sequence and the scaling exponent ν (57). Inferences from their experiments suggest that the ν ≈ 0.33 for (GRESRE)_n and ν ≈ 0.5 for (GKESKE)_n for the specific conditions they used in their measurements. Here, n is the number of repeats of the hexapeptides GRESRE or GKESKE. The results point to significant differences between Arg- and Lys-containing sequences. Further, while globularity of (GRESRE)_n has precedent in mean-field theories for polyampholytes, the mechanism by which FRC-like behavior of (GKESKE)_n is achieved is unclear. Here, we develop a plausible physical explanation for the findings of Sørensen and Kjaergaard (57). Our work is based on atomistic simulations and the ABSINTH implicit solvation model and forcefield paradigm (58–61).     

From the Cover: The evolution of parasitism from mutualism in wasps pollinating the fig,Ficus microcarpa,in Yunnan Province,China

Theory identifies factors that can undermine the evolutionary stability of mutualisms. However, theory’s relevance to mutualism stability in nature is controversial. Detailed comparative studies of parasitic species that are embedded within otherwise mutualistic taxa (e.g., fig pollinator wasps) can identify factors that potentially promote or undermine mutualism stability. We describe results from behavioral, morphological, phylogenetic, and experimental studies of two functionally distinct, but closely related, Eupristina wasp species associated with the monoecious host fig, Ficus microcarpa, in Yunnan Province, China. One (Eupristina verticillata) is a competent pollinator exhibiting morphologies and behaviors consistent with observed seed production. The other (Eupristina sp.) lacks these traits, and dramatically reduces both female and male reproductive success of its host. Furthermore, observations and experiments indicate that individuals of this parasitic species exhibit greater relative fitness than the pollinators, in both indirect competition (individual wasps in separate fig inflorescences) and direct competition (wasps of both species within the same fig). Moreover, phylogenetic analyses suggest that these two Eupristina species are sister taxa. By the strictest definition, the nonpollinating species represents a “cheater” that has descended from a beneficial pollinating mutualist. In sharp contrast to all 15 existing studies of actively pollinated figs and their wasps, the local F. microcarpa exhibit no evidence for host sanctions that effectively reduce the relative fitness of wasps that do not pollinate. We suggest that the lack of sanctions in the local hosts promotes the loss of specialized morphologies and behaviors crucial for pollination and, thereby, the evolution of cheating.

Mutualisms are defined by the net benefits that are usually provided to individuals of each interacting species. These interactions often have influences far beyond the partner species directly interacting, and commonly provide many fundamental ecosystem services (1, 2). For example, in most cases, mycorrhizal fungi provide nutrients to forest trees, pollinators help flowering plants set fruit, intestinal bacteria promote nutrient uptake across diverse animal taxa, bacteria in lucinid clams help detoxify benthic sediments, and photosynthetic algae help maintain the coral reefs that structure nearshore marine environments around the world (3–6).However, while both partners in a mutualism usually receive net benefits from the interaction, mutualisms also usually impose costs on one or both partners interacting mutualistically. In the absence of fitness-aligning mechanisms between the partners (e.g., vertical transmission of symbionts, or repeated interactions with immediate fitness benefits), theory suggests that other mechanisms are needed to maintain a mutualism’s stability. Specifically, it has been proposed that a mutualism’s long-term stability often depends on mechanisms that limit the invasion of “cheater” individuals into the populations of either partner species (2, 3, 7–14). Broadly, cheaters can be defined as individuals (or species) that do not provide a beneficial service to their partners. By not providing a potentially costly service to their partners, cheaters are thought to benefit themselves relative to “cooperating” individuals or species in the short term (12–14). Invasion by such cheaters potentially erodes the net benefits resulting from the interaction, and therefore can lead to a breakdown of the mutualism itself.Consistent with this viewpoint, data suggest that in many cases the hosts (the larger of the two partners in the mutualism) can effectively promote cooperation by selectively allocating more resources to those symbionts that provide them with greater benefits. For example, some legumes have been shown to selectively allocate more resources to nodules containing rhizobia that are better at providing fixed nitrogen (14–16). In other studies, some host plants allocate more carbon to strains of mycorrhizal fungi that provide their hosts with more phosphorus (17–19).However, other authors question the biological relevance of much of this experimental evidence to natural species interactions, the direction of cause and effect, and the actual costs for providing benefits. A central question is the degree to which evidence for cheaters, defined as receiving fitness benefits by not providing services (relative to a mutualist that does provide benefits), exist at all (12, 13, 20). Key empirical issues concern whether or not individuals with a cheating phenotype do, in fact, cheat (impose a reproductive cost on their partner, relative to a cooperating mutualist). In addition, are cheating individuals that fail to benefit their host at least as fit as cooperating (mutualistic) individuals that do? Does the host allocate relatively more resources to more beneficial partners (effectively expressing sanctions against cheaters relative to cooperators)? Ultimately, this becomes a set of specific empirical questions: What is the relative fitness of cooperators and cheaters that interact with the same partner (host)? And, does the host effectively sanction cheaters relative to cooperators, and if so, to what degree (21, 22)? At a fundamental level, the relative fitness of cheaters and cooperators is only measurable and relevant within the context of a given host’s responses to them (3, 21, 22).To resolve these questions, it is useful to study those mutualistic host–symbiont interactions in which it is straightforward to measure and experimentally manipulate both benefits and costs to each partner under natural conditions (22–32). Ideally, we should be able to comparatively assess experimental results across a diversity of host–symbiont mutualisms that differ in what theory suggests should be key metrics (e.g., strength of host sanctions, existence and relative abundance of cheaters, and so forth).The over 750 species of host figs (Ficus: Moraceae) and their obligately pollinating wasps (Agaonidae: Hymenoptera) provide such a range of both experimental and comparative options that can be exploited to address these questions (22–32) (SI Appendix, Supplementary Text and Fig. S1). Ovipositing female fig wasps deposit a drop of fluid from their poison sac into the ovules of flowers into which they lay their eggs. This fluid initiates the formation of gall tissue upon which the developing larvae feed (33) (SI Appendix). At any given site, each fig species is typically pollinated by only one or two fig wasp species (24, 26). Morphological and molecular studies broadly support coevolution between genera of pollinating wasps and their respective sections of figs, while functional studies demonstrate coadaptation between them (33–51).For example, different groups of figs are characterized by either active or passive pollination (43–45) (SI Appendix). Passive pollination does not require specialized wasp morphologies or behaviors. In contrast, active pollination requires specialized female wasp morphologies and behaviors (44). The wasps collect pollen in their natal fig using coxal combs on their forelegs and store it in pollen pockets on their thoraxes (Fig. 1). After emerging from their natal figs, female wasps use volatile chemical scent cues produced by receptive figs to identify them (35–37). Dispersal flights from the natal fig are aided by prevailing winds and routinely cover scores of kilometers (38–41). Upon finding and entering a receptive fig of an appropriate host species, the foundress wasps repeatedly remove a few grains of pollen from their pockets and place them on the stigmatic surfaces of the individual flowers on which they attempt to lay eggs. Active pollination provides clear benefits for the host fig. Pollination is more efficient in actively pollinated fig species relative to passively pollinated species. This is reflected in the dramatically lower (∼1/10) amounts of pollen that active species typically produce (43–45). Conversely, active pollination appears to be costly for the wasps in terms of specialized body structures, energy, and time (22, 42, 45).Open in a separate windowFig. 1.Receptive F. microcarpa fig and pollinating structures of E. verticillata compared with Eupristina sp. (A) A cheater wasp (Eupristina sp.) laying eggs in a receptive fig of her host F. microcarpa. Pollinator wasps (E. verticillata) (B and C) have specialized morphological structures such as pollen pockets (black arrow) on the underside of their thorax and coxal combs on their forelegs (white arrows) that facilitate pollination. Pollen is stored in the pockets and coxal combs facilitate pollen transfer (43, 44). Cheater wasps (Eupristina sp.) (D and E) retain pollen pockets (black arrow) but lack coxal combs (white arrow).The most basic mutualistic services (e.g., the wasp’s ability to pollinate) can be experimentally manipulated. By allowing or restricting the female pollinator wasps’ access to, and ability to actively collect pollen, pollinators that either do (P+) or do not (P−) carry pollen can be produced and then introduced into receptive figs (22). Furthermore, the effects on pollinator wasp fitness (i.e., lifetime reproductive success) of pollinating the host fig (or not) can be quantified by counting their relative number of offspring in naturally occurring figs (22–32). Moreover, the many existing experimental studies using the same methodologies provide context for the findings of any given experiment (22–32). In previous experiments on actively pollinated fig species, wasps that do not pollinate (P−) have lower fitness than wasps that pollinate (P+) due to increased rates of fig abortion (killing all wasp larvae) and increased larval mortality reducing the number of P− offspring that emerge. These “host sanctions” are likely caused by selective resource allocation by the tree to better-pollinated figs (28). Although pollination typically leads to a higher number of wasp offspring, pollination is not an absolute requirement for wasp offspring to develop (28). Finally, there are at least two known cases of cheating wasp species, in which species of wasps that lack both morphologies and behaviors that permit efficient, active pollination of their host co-occur with a congeneric pollinator possessing these traits. Importantly, the species that lack these traits have clearly evolved within lineages of wasps that otherwise possess these apparently costly traits that permit them to actively pollinate their host (52, 53) (SI Appendix).Here, we exploit the opportunity provided by a third case (54, 55), in which a mutualistic active pollinator and a congeneric cheater species co-occur on the same monoecious host fig. Specifically, we conducted a combination of behavioral, morphological, phylogenetic, and experimental studies to compare these wasps and the outcomes of their interactions with their shared host fig, Ficus microcarpa (subgenus Urostigma: section Urostigma: subsection Conosycea), in and near the Xishuangbanna Tropical Botanical Garden (XTBG), China. Eupristina verticillata is the described active pollinator of F. microcarpa at this location, while an undescribed coexisting wasp species (Eupristina sp.) lacks the necessary adaptation for active pollination and appears to be a cheater (54, 55).In this study, we address and answer the following questions: 1) Does the undescribed Eupristina sp. wasp associated with F. microcarpa impose a reproductive cost on its host? We find that it does, and that the cost for host reproductive success is large. 2) Does the cheater exhibit significantly higher levels of reproductive success than the pollinator in their host? Yes, in both direct and indirect competition. Combined with the reproductive loss it imposes on the host, this species meets the strictest definition of cheater. 3) Is this cheater closely related (possibly a sister species) to the mutualist pollinator of their shared host? We find that within the context of other sympatric Eupristina species associated with seven fig hosts in this area, it is. Furthermore, it represents an independent loss of pollination structures from another case previously reported in this genus. 4) Does the host (F. microcarpa) locally exhibit detectable host sanctions against wasps that do not pollinate it? In sharp contrast with all 15 other cases of actively pollinated Ficus species that have been reported (22, 29–32), we find that it does not. 5) Given that cheaters exhibit equal or greater fitness than the pollinator, how do they coexist? Although deserving further study, we suggest that regular seasonal fluctuations in the relative abundances of the two wasp species facilitate their coexistence at this site (54, 55). Seasonal changes in the prevalence of westerly winds cause regional spatial heterogeneity in source pools of pollinators and cheaters that immigrate to the local host, F. microcarpa.     

Ancestral polymorphisms shape the adaptive radiation of Metrosideros across the Hawaiian Islands

Some of the most spectacular adaptive radiations begin with founder populations on remote islands. How genetically limited founder populations give rise to the striking phenotypic and ecological diversity characteristic of adaptive radiations is a paradox of evolutionary biology. We conducted an evolutionary genomics analysis of genus Metrosideros, a landscape-dominant, incipient adaptive radiation of woody plants that spans a striking range of phenotypes and environments across the Hawaiian Islands. Using nanopore-sequencing, we created a chromosome-level genome assembly for Metrosideros polymorpha var. incana and analyzed whole-genome sequences of 131 individuals from 11 taxa sampled across the islands. Demographic modeling and population genomics analyses suggested that Hawaiian Metrosideros originated from a single colonization event and subsequently spread across the archipelago following the formation of new islands. The evolutionary history of Hawaiian Metrosideros shows evidence of extensive reticulation associated with significant sharing of ancestral variation between taxa and secondarily with admixture. Taking advantage of the highly contiguous genome assembly, we investigated the genomic architecture underlying the adaptive radiation and discovered that divergent selection drove the formation of differentiation outliers in paired taxa representing early stages of speciation/divergence. Analysis of the evolutionary origins of the outlier single nucleotide polymorphisms (SNPs) showed enrichment for ancestral variations under divergent selection. Our findings suggest that Hawaiian Metrosideros possesses an unexpectedly rich pool of ancestral genetic variation, and the reassortment of these variations has fueled the island adaptive radiation.

Adaptive radiations exhibit extraordinary levels of morphological and ecological diversity (1). Although definitions of adaptive radiation vary (2–7), all center on ecological opportunity as a driver of adaptation and, ultimately, diversification (2, 8–10). Divergent selection, the primary mechanism underlying adaptive radiations, favors extreme phenotypes (11) and selects alleles that confer adaptation to unoccupied or under-utilized ecological niches. Differential adaptation results in divergence and, ultimately, reproductive isolation between populations (12). Adaptive radiations demonstrate the remarkable power of natural selection as a driver of biological diversity and provide excellent systems for studying evolutionary processes involved in diversification and speciation (13).Adaptive radiations on remote oceanic islands are especially interesting, as colonization of remote islands is expected to involve population bottlenecks that restrict genetic variation (14). Adaptive radiations in such settings are especially impressive and even paradoxical, given the generation of high species richness from an initially limited gene pool (15). Several classic examples of adaptive radiation occur on oceanic islands, such as Darwin’s finches from the Galapagos islands (16), anole lizards from the Caribbean islands (9), Hawaiian Drosophilids (17), and Hawaiian silverswords (18), to name a few.Recent advances in genome sequencing and analyses have greatly improved our ability to examine the genetics of speciation and adaptive radiation. By examining sequences of multiple individuals from their natural environment, it has become possible to “catch in the act” the speciation processes between incipient lineages (19). Genomic studies of early stage speciation show that differentiation accumulates in genomic regions that restrict the homogenizing effects of gene flow between incipient species (20). The number, size, and distribution of these genomic regions can shed light on evolutionary factors involved in speciation (19). Regions of high genomic differentiation can also form from evolutionary factors unrelated to speciation, such as linkage associated with recurrent background selection or selective sweeps on shared genomic features (21, 22).Genomic studies of lineages undergoing rapid ecological diversification have begun to reveal the evolutionary mechanisms underlying adaptive radiations. Importantly, these studies highlight the pivotal role of hybridization between populations and the consequent exchange of adaptive alleles that facilitates rapid speciation and the colonization of diverse niches (23–25). Most genomic studies of adaptive radiation involve animal systems, however, in particular, birds and fishes. In plants, genomic studies of adaptive radiation are sparse (26–28), and all examine continent-wide radiations. There are no genomics studies of plant adaptive radiations in geographically restricted systems such as remote islands. Because the eco-evolutionary scenarios associated with adaptive radiations are diverse (5, 29), whether commonalities identified in adaptive radiations in animals (23, 30) are applicable to plants is an open question. For example, the genetic architecture of animal adaptive radiations typically involves differentiation at a small number of genomic regions (31–33). In contrast, the limited insights available for plants suggest a more complex genetic architecture (26).We investigated the evolutionary genomics of adaptive radiation in Metrosideros Banks ex Gaertn. (Myrtaceae) across the Hawaiian Islands. Hawaiian Metrosideros is a landscape-dominant, hypervariable, and highly dispersible group of long-lived (possibly >650 y) (34) woody taxa that are nonrandomly distributed across Hawaii’s heterogeneous landscape, including cooled lava flows, wet forests and bogs, subalpine zones, and riparian zones (35, 36). About 25 taxa or morphotypes are distinguished by vegetative characters ranging from prostate plants that flower a few centimeters above ground to 30-m-tall trees, and leaves range dramatically in size, shape, pubescence, color, and rugosity (35, 37, 38); a majority of these forms are intraspecific varieties or races (provisional varieties) of the abundant species, Metrosideros polymorpha (35, 36, 38). Variation in leaf mass per area within the four Metrosideros taxa on Hawaii Island alone matches that observed for woody species globally (39). Common garden experiments (38, 40–44) and parent–offspring analysis (45) demonstrate heritability of taxon-diagnostic vegetative traits, indicating that taxa are distinct genetic groups and not the result of phenotypic plasticity. Metrosideros taxa display evidence of local adaptation to contrasting environments (46, 47), suggesting ecological divergent selection is responsible for diversification within the group (48). This diversification, which spans the past ∼3.1 to 3.9 million years (49, 50), has occurred despite the group’s high capacity for gene flow by way of showy bird-pollinated flowers and tiny wind-dispersed seeds (36, 51). Lastly, the presence of partial reproductive isolating barriers between taxa is consistent with the early stages of speciation (52). Here, we generated several genomic resources for Hawaiian Metrosideros and used these in population genomics analyses to gain deeper insights into the genomic architecture and evolutionary processes underlying this island adaptive radiation.     

INAUGURAL ARTICLE by a Recently Elected Academy Member:Synergistic regulation of nonbinary molecular switches by protonation and light

We report a molecular switching ensemble whose states may be regulated in synergistic fashion by both protonation and photoirradiation. This allows hierarchical control in both a kinetic and thermodynamic sense. These pseudorotaxane-based molecular devices exploit the so-called Texas-sized molecular box (cyclo[2]-(2,6-di(1H-imidazol-1-yl)pyridine)[2](1,4-dimethylenebenzene); 1⁴⁺, studied as its tetrakis-PF₆ ⁻ salt) as the wheel component. Anions of azobenzene-4,4′-dicarboxylic acid (2H⁺•2) or 4,4′-stilbenedicarboxylic acid (2H⁺•3) serve as the threading rod elements. The various forms of 2 and 3 (neutral, monoprotonated, and diprotonated) interact differently with 1⁴⁺, as do the photoinduced cis or trans forms of these classic photoactive guests. The net result is a multimodal molecular switch that can be regulated in synergistic fashion through protonation/deprotonation and photoirradiation. The degree of guest protonation is the dominating control factor, with light acting as a secondary regulatory stimulus. The present dual input strategy provides a complement to more traditional orthogonal stimulus-based approaches to molecular switching and allows for the creation of nonbinary stimulus-responsive functional materials.

Multifactor regulation of biomolecular machines is essential to their ability to carry out various biological functions (1 –11). Construction of artificial molecular devices with multifactor regulation features may allow us to understand and simulate biological systems more effectively (12 –31). However, creating and controlling such synthetic constructs remains challenging (16, 32 –37). Most known systems involving multifactor regulation, including most so-called molecular switches and logic devices (38 –43), have been predicated on an orthogonal strategy wherein the different control factors that determine the distribution of accessible states do not affect one another (20, 44 –56). However, in principle, a greater level of control can be achieved by using two separate regulatory inputs that operate in synergistic fashion. Ideally, this could lead to hierarchical control where different states are specifically accessed by means of appropriately selected nonorthogonal inputs. However, to our knowledge, only a limited number of reports detailing controlled hierarchical systems have appeared (57). Furthermore, the balance between specific effects (e.g., kinetics vs. thermodynamics) under conditions of stimulus regulation is still far from fully understood (54). There is thus a need for new systems that can provide further insights into the underlying design determinants. Here we report a set of pseudorotaxane molecular shuttles that act as multimodal chemical switches subject to hierarchical control.     

Combining pressure and electrochemistry to synthesize superhydrides

Recently, superhydrides have been computationally identified and subsequently synthesized with a variety of metals at very high pressures. In this work, we evaluate the possibility of synthesizing superhydrides by uniquely combining electrochemistry and applied pressure. We perform computational searches using density functional theory and particle swarm optimization calculations over a broad range of pressures and electrode potentials. Using a thermodynamic analysis, we construct pressure–potential phase diagrams and provide an alternate synthesis concept, pressure–potential (P2), to access phases having high hydrogen content. Palladium–hydrogen is a widely studied material system with the highest hydride phase being Pd₃H₄. Most strikingly for this system, at potentials above hydrogen evolution and ∼ 300 MPa pressure, we find the possibility to make palladium superhydrides (e.g., PdH₁₀). We predict the generalizability of this approach for La-H, Y-H, and Mg-H with 10- to 100-fold reduction in required pressure for stabilizing phases. In addition, the P2 strategy allows stabilizing additional phases that cannot be done purely by either pressure or potential and is a general approach that is likely to work for synthesizing other hydrides at modest pressures.

Hydrides are a large class of materials containing hydrogen, the lightest and most abundant element in the universe. They have attracted much research interest due to their scientific significance and numerous applications. As important hydrogen storage media (1), they are able to store hydrogen at densities higher than that of liquid hydrogen (2). They also find applications in hydrogen compressors (3), refrigeration (4), heat storage (5), thermal engines (6), batteries (7), fuel cells (8), actuators (9), gas sensors (10), smart windows (11), H₂ purification (12), isotope separation (13), alloy processing (14), catalysis (15), semiconductors (16), neutron moderators (17), low-energy nuclear reactions (18), and recently possible high-temperature superconductors with a critical superconducting temperature T_c in the vicinity of room temperature in hydrogen-rich materials under pressure (19–38).In the late 1960s, Neil Ashcroft (19) and Vitaly Ginzburg (20) independently considered the possibility of high-temperature superconductivity in metallic solid hydrogen at high pressure. Later, the idea of chemical precompression was proposed in which chemical “pressure” is exerted to form hydrogen dominant metal hydrides stable at lower pressures (21). Following the successful prediction (22, 23) and confirmation (24) of very high T_c superconductivity in H₃S, near–room-temperature superconductivity was predicted (25, 26), synthesized (27), and discovered (28) in the superhydrides (defined as MH_n, for n > 6) in the La-H system. Later, comparable T_c values were observed experimentally for other La-H (29), Y-H (30–32), and La-Y-H (33) superhydrides, and room-temperature superconductivity was also reported in the C-S-H system (34). In addition, even higher T_c s have been theoretically predicted, such as Li₂MgH₁₆ with T_c as high as ∼ 470 K at 250 GPa (35).High pressures are needed to synthesize superhydrides (38). One major reason is that at lower pressures, the thermodynamic stability of superhydrides is weakened or no longer exists. To overcome such a challenge, it is obvious that more processing variables need to be introduced in addition to chemical composition and pressure. A processing variable that has been largely hidden is the electrical potential when utilizing electrochemistry for synthesis, which has been used in synthesizing palladium hydride at ambient pressure (39). In the present work we show that the synergetic use of pressure and electrical potential can dramatically extend the thermodynamic stability regime of superhydrides to modest pressures, an approach we term P2. This approach opens more opportunities for the creation of superhydrides and other materials by combining pressure and electrochemical loading techniques. We begin by outlining the general thermodynamic framework. We then apply the approach to the Pd-H system, where we also present density functional theory (DFT) predictions of palladium hydrides under pressure. This is followed by predictions for other metal hydride systems and then a discussion of the broad implications.