Fluctuations in density of an outbreak species drive diversity cascades in food webs

Patterns in food-web structure have frequently been examined in static food webs, but few studies have attempted to delineate patterns that materialize in food webs under nonequilibrium conditions. Here, using one of nature's classical nonequilibrium systems as the food-web database, we test the major assumptions of recent advances in food-web theory. We show that a complex web of interactions between insect herbivores and their natural enemies displays significant architectural flexibility over a large fluctuation in the natural abundance of the major herbivore, the spruce budworm (Choristoneura fumiferana). Importantly, this flexibility operates precisely in the manner predicted by recent foraging-based food-web theories: higher-order mobile generalists respond rapidly in time and space by converging on areas of increasing prey abundance. This "birdfeeder effect" operates such that increasing budworm densities correspond to a cascade of increasing diversity and food-web complexity. Thus, by integrating foraging theory with food-web ecology and analyzing a long-term, natural data set coupled with manipulative field experiments, we are able to show that food-web structure varies in a predictable manner. Furthermore, both recent food-web theory and longstanding foraging theory suggest that this very same food-web flexibility ought to be a potent stabilizing mechanism. Interestingly, we find that this food-web flexibility tends to be greater in heterogeneous than in homogeneous forest plots. Because our results provide a plausible mechanism for boreal forest effects on populations of forest insect pests, they have implications for forest and pest management practices.     

Evolutionary diversification of the multimeric states of proteins

One of the most striking features of proteins is their common assembly into multimeric structures, usually homomers with even numbers of subunits all derived from the same genetic locus. However, although substantial structural variation for orthologous proteins exists within and among major phylogenetic lineages, in striking contrast to patterns of gene structure and genome organization, there appears to be no correlation between the level of protein structural complexity and organismal complexity. In addition, there is no evidence that protein architectural differences are driven by lineage-specific differences in selective pressures. Here, it is suggested that variation in the multimeric states of proteins can readily arise from stochastic transitions resulting from the joint processes of mutation and random genetic drift, even in the face of constant directional selection for one particular protein architecture across all lineages. Under the proposed hypothesis, on a long evolutionary timescale, the numbers of transitions from monomers to dimers should approximate the numbers in the opposite direction and similarly for transitions between higher-order structures.Given the cellular basis of life, a fully synthetic theory of evolution will ultimately require an understanding of the population-genetic mechanisms influencing heritable changes in cell features. As much of cellular infrastructure is composed of proteins, such an enterprise should arguably begin with the evolutionary dynamics of protein structure. Remarkably, however, one of the most striking features of proteins across the tree of life is almost completely unexplored from an evolutionary perspective. Only a minority of proteins function as isolated units. Instead, most exist as symmetrical higher-order complexes composed of subunits encoded by the same locus. Depending on the numbers of subunits, such complexes are referred to as homodimers, homotrimers, homotetramers, etc. Understanding the emergence of such liaisons is a central issue in the nascent field of evolutionary cell biology.Most attempts to explain the existence of multimers have started with the implicit assumption that their origin and retention are a consequence of adaptive evolution (1–5), and the resultant proposed advantages are not in short supply. First, it is generally easier to fold multiple small proteins than a single long one, although this does not explain the very large fraction of multimers retaining active sites within each subunit (as opposed to active sites being products of subunit interfaces). Second, the encounter rate of an enzyme and a small substrate is proportional to the effective radius of the enzyme (6, 7), and provided the catalytic site remains exposed, the elimination of extraneous protein surface may further enhance the frequency of productive encounters. Third, a smaller surface-area to volume ratio may reduce a protein’s vulnerability to denaturation or engagement in promiscuous interactions. Fourth, higher-order structures may reduce the sensitivity of catalytic sites to internal motions, thereby increasing substrate specificity; and oligomerization may protect otherwise unstable proteins from aggregation (8). Fifth, complexation offers increased opportunities for allosteric regulation of protein activity.Although the large pool of oligomeric structures in today’s organisms cannot possibly be strongly maladaptive, this need not imply that they have arisen by or are currently maintained by adaptive processes. Indeed, despite the plausibility of many of the above hypotheses, empirical evidence for the adaptive value of alternative multimeric structures is essentially completely lacking, and a number of examples can be pointed to in which a more complex structure seemingly operates no more efficiently in its lineage than a simpler structure in others (9, 10). Moreover, the transition to an oligomerized state imposes clear challenges. First, to achieve a critical concentration of an active multimer, the expression of monomeric subunits must be raised to a high enough level to ensure an adequate number of encounters for successful complex assembly. This increase in subunit production will entail an energetic cost. Second, unless a newly emerging dimer has a symmetric interface and the correct subunit orientation, concatenations into indefinite filaments can arise. Numerous human disorders are known to result from inappropriate protein aggregation (11), and highly expressed proteins are especially vulnerable to promiscuous interactions (12, 13). Third, in diploid species, some dimerizing mutations may have deleterious effects in heterozygous individuals as a consequence of heterotypic complexation, a process that can greatly reduce the probability of establishment of the dimerizing allele (10).     

Evolutionary cell biology: Two origins,one objective

All aspects of biological diversification ultimately trace to evolutionary modifications at the cellular level. This central role of cells frames the basic questions as to how cells work and how cells come to be the way they are. Although these two lines of inquiry lie respectively within the traditional provenance of cell biology and evolutionary biology, a comprehensive synthesis of evolutionary and cell-biological thinking is lacking. We define evolutionary cell biology as the fusion of these two eponymous fields with the theoretical and quantitative branches of biochemistry, biophysics, and population genetics. The key goals are to develop a mechanistic understanding of general evolutionary processes, while specifically infusing cell biology with an evolutionary perspective. The full development of this interdisciplinary field has the potential to solve numerous problems in diverse areas of biology, including the degree to which selection, effectively neutral processes, historical contingencies, and/or constraints at the chemical and biophysical levels dictate patterns of variation for intracellular features. These problems can now be examined at both the within- and among-species levels, with single-cell methodologies even allowing quantification of variation within genotypes. Some results from this emerging field have already had a substantial impact on cell biology, and future findings will significantly influence applications in agriculture, medicine, environmental science, and synthetic biology.     

Evolutionary emergence of responsive and unresponsive personalities

In many animal species, individuals differ consistently in suites of correlated behaviors, comparable with human personalities. Increasing evidence suggests that one of the fundamental factors structuring personality differences is the responsiveness of individuals to environmental stimuli. Whereas some individuals tend to be highly responsive to such stimuli, others are unresponsive and show routine-like behaviors. Much research has focused on the proximate causes of these differences but little is known about their evolutionary origin. Here, we provide an evolutionary explanation. We develop a simple but general evolutionary model that is based on two key ingredients. First, the benefits of responsiveness are frequency-dependent; that is, being responsive is advantageous when rare but disadvantageous when common. This explains why responsive and unresponsive individuals can coexist within a population. Second, positive-feedback mechanisms reduce the costs of responsiveness; that is, responsiveness is less costly for individuals that have been responsive before. This explains why individuals differ consistently in their responsiveness, across contexts and over time. As a result, natural selection gives rise to stable individual differences in responsiveness. Whereas some individuals respond to environmental stimuli in all kinds of contexts, others consistently neglect such stimuli. Interestingly, such differences induce correlations among all kinds of other traits (e.g., boldness and aggressiveness), thus providing an explanation for environment-specific behavioral syndromes.     

Adaptive evolution toward larger size in mammals

The notion that large body size confers some intrinsic advantage to biological species has been debated for centuries. Using a phylogenetic statistical approach that allows the rate of body size evolution to vary across a phylogeny, we find a long-term directional bias toward increasing size in the mammals. This pattern holds separately in 10 of 11 orders for which sufficient data are available and arises from a tendency for accelerated rates of evolution to produce increases, but not decreases, in size. On a branch-by-branch basis, increases in body size have been more than twice as likely as decreases, yielding what amounts to millions and millions of years of rapid and repeated increases in size away from the small ancestral mammal. These results are the first evidence, to our knowledge, from extant species that are compatible with Cope’s rule: the pattern of body size increase through time observed in the mammalian fossil record. We show that this pattern is unlikely to be explained by several nonadaptive mechanisms for increasing size and most likely represents repeated responses to new selective circumstances. By demonstrating that it is possible to uncover ancient evolutionary trends from a combination of a phylogeny and appropriate statistical models, we illustrate how data from extant species can complement paleontological accounts of evolutionary history, opening up new avenues of investigation for both.The idea that large size confers some intrinsic advantage has lingered in the psyche of biologists for centuries. Researchers have proposed that bigger body sizes can increase tolerance to environmental extremes (1), reduce mortality (2), and enhance predation success (3), among other advantages. In support of these conjectures, analyses from a range of different taxonomic groups demonstrate that larger individuals within populations have significantly enhanced survival, fecundity, and mating success (4, 5). If these advantages are general and have played out over long time scales, they could explain the existence of Cope’s rule (6): a broad trend toward increasing size through time (4, 5, 7).Mammals evolved from a relatively small common ancestor over 165 Ma (8–10) and went on to form one of the largest and most successful vertebrate radiations in Earth’s history. Mammals vary greatly in size, spanning almost eight orders of magnitude. This variation implies that some groups have experienced much greater evolutionary change in size from the ancestral form than others. Indeed, the mammalian fossil record provides the clearest evidence in support of Cope’s rule over long evolutionary time scales (6, 11, 12).Despite the paleontological support, evidence for Cope’s rule remains elusive from studies of extant data alone (13–15), including studies of the mammals (16). A possible reason for the discrepancy between paleontological and extant data might be that conventional comparative methods for studying trends within extant data implicitly assume homogeneous evolutionary patterns and processes. When these assumptions are violated, it renders the homogeneous modeling approach incomplete at best and at worst, a source of potential bias in the study of historical evolutionary change; for example, reconstructions of probable ancestral values can be biased toward average or intermediate values (17, 18), which would thereby mask long-term evolutionary trends that are apparent from the fossil record.Previously, we have shown that rates of body size evolution in mammals routinely violate the assumption of homogeneity (19), but how these rate changes might be related to size itself has not been studied. If changes toward larger size in the mammals have consistently occurred at rates that differ from changes toward smaller size, then reconstructed ancestral states accounting for these rate differences may track more closely the observed fossil record. Such a pattern would allow the detection of size-related evolutionary trends from extant data (Fig. S1).Here, we apply a statistical phylogenetic approach for reconstructing mammalian evolutionary history that allows the rate of evolution to vary throughout a phylogenetic tree without prior knowledge or specification of where and when rate shifts occurred. We use this method to test for size-related biases in rates of morphological change and ask whether accounting for any such bias allows us to predict a generalized pattern of size increase in the mammals in line with the generalized pattern of size increase observed in the fossil record. Finally, we consider whether a size-related bias in the rate of morphological evolution can help to choose among the several macroevolutionary processes that have been suggested to give rise to Cope’s rule.     

Evolutionary analyses of non-genealogical bonds produced by introgressive descent

All evolutionary biologists are familiar with evolutionary units that evolve by vertical descent in a tree-like fashion in single lineages. However, many other kinds of processes contribute to evolutionary diversity. In vertical descent, the genetic material of a particular evolutionary unit is propagated by replication inside its own lineage. In what we call introgressive descent, the genetic material of a particular evolutionary unit propagates into different host structures and is replicated within these host structures. Thus, introgressive descent generates a variety of evolutionary units and leaves recognizable patterns in resemblance networks. We characterize six kinds of evolutionary units, of which five involve mosaic lineages generated by introgressive descent. To facilitate detection of these units in resemblance networks, we introduce terminology based on two notions, P3s (subgraphs of three nodes: A, B, and C) and mosaic P3s, and suggest an apparatus for systematic detection of introgressive descent. Mosaic P3s correspond to a distinct type of evolutionary bond that is orthogonal to the bonds of kinship and genealogy usually examined by evolutionary biologists. We argue that recognition of these evolutionary bonds stimulates radical rethinking of key questions in evolutionary biology (e.g., the relations among evolutionary players in very early phases of evolutionary history, the origin and emergence of novelties, and the production of new lineages). This line of research will expand the study of biological complexity beyond the usual genealogical bonds, revealing additional sources of biodiversity. It provides an important step to a more realistic pluralist treatment of evolutionary complexity.     

Evolutionary divergence of duplicated genomes in newly described allotetraploid cottons

Allotetraploid cotton (Gossypium) species represents a model system for the study of plant polyploidy, molecular evolution, and domestication. Here, chromosome-scale genome sequences were obtained and assembled for two recently described wild species of tetraploid cotton, Gossypium ekmanianum [(AD)₆, Ge] and Gossypium stephensii [(AD)₇, Gs], and one early form of domesticated Gossypium hirsutum, race punctatum [(AD)₁, Ghp]. Based on phylogenomic analysis, we provide a dated whole-genome level perspective for the evolution of the tetraploid Gossypium clade and resolved the evolutionary relationships of Gs, Ge, and domesticated G. hirsutum. We describe genomic structural variation that arose during Gossypium evolution and describe its correlates—including phenotypic differentiation, genetic isolation, and genetic convergence—that contributed to cotton biodiversity and cotton domestication. Presence/absence variation is prominent in causing cotton genomic structural variations. A presence/absence variation-derived gene encoding a phosphopeptide-binding protein is implicated in increasing fiber length during cotton domestication. The relatively unimproved Ghp offers the potential for gene discovery related to adaptation to environmental challenges. Expanded gene families enoyl-CoA δ isomerase 3 and RAP2-7 may have contributed to abiotic stress tolerance, possibly by targeting plant hormone-associated biochemical pathways. Our results generate a genomic context for a better understanding of cotton evolution and for agriculture.

Polyploidization is an important evolutionary process in many higher plants, contributing to speciation and adaptation (1–5). Allopolyploidy in particular has been considered a major evolutionary force due to the novel genomic possibilities resulting from hybridization and increased genetic variability. Approximately 1 to 2 million y ago (Mya), hybridization between geographically disjunct diploid A and D genome ancestors (2n = 26, AA and DD genome) and concomitant polyploidization generated allotetraploid cotton (2n = 52, AADD genome) (6, 7). This new allopolyploid clade subsequently diversified into the seven species recognized today [(AD)₁ to (AD)₇] (8, 9). Among them, Gossypium hirsutum [Gh, genome designation (AD)₁] and Gossypium barbadense [Gb, (AD)₂)], provide the majority of natural fiber for commercial production (10, 11). Five tetraploid cottons [(AD)₁ to (AD)₅], including the two domesticated species, have recently been sequenced using long-read technology, providing high-quality genome assemblies and genomic resources for uncovering the genetic basis of spinnable fiber (12–16). However, genome assemblies for the two most recently described wild tetraploid species, both of which are closely related to Gh, have not been reported. Genome sequences for these species may facilitate an improved understanding of evolution and fiber improvement in the dominant crop species, G. hirsutum. In fact, these species—that is, Gossypium ekmanianum [Ge, (AD)₆] from the Dominican Republic and Gossypium stephensii [Gs, (AD)₇] from the Wake Atoll near French Polynesia—are so similar to Gh that they have historically been confounded with wild accessions of Gh (8, 9). Additionally, there are no genome sequences for early domesticated or wild forms of either of the two domesticated species, precluding comparative genomic approaches to understanding cotton evolution and domestication. Among the great diversity of morphological forms spanning the wild-to-domesticated continuum in Gh, many of the least-improved forms occur in the Yucatan Peninsula of Mexico, including the truly wild race yucatanense, and the relatively unimproved race punctatum (Ghp) (17, 18). Assembling the genome of these tetraploid cottons will provide an important model system for understanding both the evolutionary consequences of polyploidy and of parallel domestication (19–21).Here, we report high-quality genome assemblies of the three tetraploid genomes, Ge, Gs, and Ghp. Using comparative genomics and phylogenomics, we reveal extensive genomic structural variations (SVs) in tetraploid cottons, and reevaluate phylogenetic relationships and divergence times within the polyploid clade. Extensive SVs are associated with phenotypic diversity, including the economically important trait, fiber length. We characterize wild gene resources that have the potential to facilitate adaptation to various abiotic and biotic stresses in domesticated cotton. These results deepen our understanding of genome evolution in polyploids and provide insight into the genetic and morphological diversity of tetraploid cottons.     

Resonance-induced multimodal body-size distributions in ecosystems

The size of an organism reflects its metabolic rate, growth rate, mortality, and other important characteristics; therefore, the distribution of body size is a major determinant of ecosystem structure and function. Body-size distributions often are multimodal, with several peaks of abundant sizes, and previous studies suggest that this is the outcome of niche separation: species from distinct peaks avoid competition by consuming different resources, which results in selection of different sizes in each niche. However, this cannot explain many ecosystems with several peaks competing over the same niche. Here, we suggest an alternative, generic mechanism underlying multimodal size distributions, by showing that the size-dependent tradeoff between reproduction and resource utilization entails an inherent resonance that may induce multiple peaks, all competing over the same niche. Our theory is well fitted to empirical data in various ecosystems, in which both model and measurements show a multimodal, periodically peaked distribution at larger sizes, followed by a smooth tail at smaller sizes. Moreover, we show a universal pattern of size distributions, manifested in the collapse of data from ecosystems of different scales: phytoplankton in a lake, metazoans in a stream, and arthropods in forests. The demonstrated resonance mechanism is generic, suggesting that multimodal distributions of numerous ecological characters emerge from the interplay between local competition and global migration.     

Scaling expectations for the time to establishment of complex adaptations

Although the vast majority of research in evolutionary biology is focused on adaption, a general theory for the population-genetic mechanisms by which complex adaptations are acquired remains to be developed. The issue explored here is the procurement of novel traits that specifically require multiple mutations to achieve a fitness advantage. By highlighting the roles played by the forces of mutation, recombination, and random genetic drift, and drawing from observations on the joint constraints on these factors, the ways in which rates of acquisition of specific types of adaptations scale with population size are explored. These general results provide insight into a number of ongoing controversies regarding the molecular basis of adaptation, including the adaptive utility of recombination and the role of drift in the passage through adaptive valleys.     

The rise of biting during the Cenozoic fueled reef fish body shape diversification

Diversity of feeding mechanisms is a hallmark of reef fishes, but the history of this variation is not fully understood. Here, we explore the emergence and proliferation of a biting mode of feeding, which enables fishes to feed on attached benthic prey. We find that feeding modes other than suction, including biting, ram biting, and an intermediate group that uses both biting and suction, were nearly absent among the lineages of teleost fishes inhabiting reefs prior to the end-Cretaceous mass extinction, but benthic biting has rapidly increased in frequency since then, accounting for about 40% of reef species today. Further, we measured the impact of feeding mode on body shape diversification in reef fishes. We fit a model of multivariate character evolution to a dataset comprising three-dimensional body shape of 1,530 species of teleost reef fishes across 111 families. Dedicated biters have accumulated over half of the body shape variation that suction feeders have in just 18% of the evolutionary time by evolving body shape ∼1.7 times faster than suction feeders. As a possible response to the ecological and functional diversity of attached prey, biters have dynamically evolved both into shapes that resemble suction feeders as well as novel body forms characterized by lateral compression and small jaws. The ascendance of species that use biting mechanisms to feed on attached prey reshaped modern reef fish assemblages and has been a major contributor to their ecological and phenotypic diversification.

Reef habitats are renowned for high biodiversity (1–5). Often, this pattern is attributed to the structural complexity of reefs, as complex habitats provide increased opportunity for microhabitat-related adaptations and niche partitioning (6–8). Among reef fishes, many major drivers of phenotypic and ecological diversity have been recognized at a range of phylogenetic scales (9–13), but we still lack a clear understanding of the processes and mechanisms that have made reef fish faunas the most diverse in modern oceans.One striking axis of diversity that distinguishes reef fish communities from those in other marine habitats is the variety of feeding modes used to capture prey. Fishes can employ a direct biting mechanism to remove attached prey from hard substrates or can use suction feeding, which relies on the density and viscosity of an aquatic medium to pull in water and prey via rapid expansion of the head. Suction feeding, which is most effectively used to capture mobile prey (14–19), is both ancestral for teleost fishes (20) and well represented on modern reefs (21). However, direct biting feeding mechanisms characterize many iconic reef fish groups, including parrotfishes, butterflyfishes, surgeonfishes, and triggerfishes. The evolution of biting has allowed fishes to exploit a variety of benthic prey that are firmly attached to reef surfaces and thus, resist suction, including molluscs, echinoderms, cnidarians, sponges, algae, and other primary producers (22–27). The ecosystem importance of this functional breakthrough in trophic habits is perhaps best represented by the many benthic biting herbivores and detritivores (27–32) that play a central role in energy transfer through reefs and regulating the composition of benthic communities (33–37).Benthic biting has been a major facet of the trophic diversity of reef fishes since at least the Eocene. Herbivores were well established in the Monte Bolca lagerstätte (∼50 Ma), marking the first evidence that teleosts could graze upon the reef surface and signaling a major shift in reef community functions (38–40). These herbivores appear to have risen to dominance within reef ecosystems globally through expansion and colonization following the split of the Tethys Sea and the increased availability of reef flat habitats in the Late Cenozoic (40–44), although the implications of biting for phenotypic diversification of reef fishes remain unknown (40). Use of a biting feeding mode prior to the Eocene appears to be primarily the domain of nonteleost fishes. As long ago as the Devonian, lungfishes and some arthrodire placoderms captured and crushed hard prey with their jaws (45–48). Several lineages of early-branching ray-finned fishes used biting for prey capture throughout the Mesozoic, including pycnodonts, macrosemiids, and semionotids (38, 49–51); of these, pycnodonts persisted until the Eocene (51). The striking lack of biting teleosts prior to the Eocene (38) may be due to a 20-My gap in major deposits of spiny-rayed (Acanthomorph) fishes from the Late Campanian (∼75 Ma) to the Late Paleocene (∼55 Ma) (52), during which biting by teleost fishes most likely proliferated to its Eocene prominence. The ambiguity regarding the origins of the expansion of biting among teleosts and its role in morphological diversification presents an opportunity for comparative phylogenetics to provide insight into the history of modern reef fishes.In this study, we explored the evolutionary history of benthic biting feeding mechanisms in reef fishes and the impact this novelty had on their phenotypic diversification. We compared benthic biting with three other feeding modes: suction feeding, an intermediate group using a mix of both suction and biting, and an uncommon feeding mode we refer to as “ram biting.” To determine how the prevalence of benthic biting has changed through time, we reconstructed the history of feeding modes among reef-dwelling teleosts using stochastic mapping on a time-calibrated phylogeny. We then measured the effect of feeding mode on rates of body shape evolution across a broad sample of 1,530 species of reef fishes spanning 111 families of extant teleosts. If biting feeding modes have been a significant stimulus to the diversification of modern reef fishes, we expect to see differences in body shape occupation of morphospace and phenotypic diversification when comparing biters with fish that employ other feeding modes. Our results provide insight into the evolutionary mechanisms underlying the vast phenotypic and ecological diversity of reef fishes.     

Simple prediction of interaction strengths in complex food webs

Darwin''s classic image of an “entangled bank” of interdependencies among species has long suggested that it is difficult to predict how the loss of one species affects the abundance of others. We show that for dynamical models of realistically structured ecological networks in which pair-wise consumer-resource interactions allometrically scale to the ¾ power—as suggested by metabolic theory—the effect of losing one species on another can be predicted well by simple functions of variables easily observed in nature. By systematically removing individual species from 600 networks ranging from 10–30 species, we analyzed how the strength of 254,032 possible pair-wise species interactions depended on 90 stochastically varied species, link, and network attributes. We found that the interaction strength between a pair of species is predicted well by simple functions of the two species'' biomasses and the body mass of the species removed. On average, prediction accuracy increases with network size, suggesting that greater web complexity simplifies predicting interaction strengths. Applied to field data, our model successfully predicts interactions dominated by trophic effects and illuminates the sign and magnitude of important nontrophic interactions.     

Iterative adaptive radiations of fossil canids show no evidence for diversity-dependent trait evolution

A long-standing hypothesis in adaptive radiation theory is that ecological opportunity constrains rates of phenotypic evolution, generating a burst of morphological disparity early in clade history. Empirical support for the early burst model is rare in comparative data, however. One possible reason for this lack of support is that most phylogenetic tests have focused on extant clades, neglecting information from fossil taxa. Here, I test for the expected signature of adaptive radiation using the outstanding 40-My fossil record of North American canids. Models implying time- and diversity-dependent rates of morphological evolution are strongly rejected for two ecologically important traits, body size and grinding area of the molar teeth. Instead, Ornstein–Uhlenbeck processes implying repeated, and sometimes rapid, attraction to distinct dietary adaptive peaks receive substantial support. Diversity-dependent rates of morphological evolution seem uncommon in clades, such as canids, that exhibit a pattern of replicated adaptive radiation. Instead, these clades might best be thought of as deterministic radiations in constrained Simpsonian subzones of a major adaptive zone. Support for adaptive peak models may be diagnostic of subzonal radiations. It remains to be seen whether early burst or ecological opportunity models can explain broader adaptive radiations, such as the evolution of higher taxa.A central prediction of modern adaptive radiation theory is that rates of diversification and phenotypic evolution are fastest early in clade history and subsequently slow as niches become saturated (1). This prediction is derived in large part from the writings of Simpson (2, 3), who suggested that fast rates of phenotypic evolution are required during the early phases of adaptive radiation to move lineages rapidly through inadaptive phases of the adaptive landscape to a new peak. Although the fossil record provides many examples of rapid early accumulation of morphological disparity (4–10), direct evidence for early rapid rates of phenotypic evolution, a so-called “early burst,” has proved rare in phylogenetic comparative data (11). There are several plausible explanations for why early bursts are seldom observed. For example, temporally declining rates are difficult to detect in datasets comprising only extant taxa, and comparative methods are extremely sensitive to noise from convergence or measurement error (11, 12). Incorporation of fossil taxa in phylogenetic tests for early bursts can improve detection of these patterns (13), although isolated analyses of subclades within a larger adaptive radiation may fail to show evidence of declining disparity with time if rates have already significantly decreased, even when fossil species are sampled (14).An alternative explanation for the lack of early bursts in comparative data is that ecological opportunity, not time, is the key determinant of rates of morphological evolution. If opportunity is the dominant force driving rates of morphological evolution in adaptive radiation, then the early burst model should be a particularly poor fit when clade age is a weak predictor of species richness. Patterns of diversity through time in the fossil record strongly suggest that diversity-dependent speciation and extinction dynamics are common (15–17) and weak or negative relationships between clade age and species richness are increasingly recognized in molecular phylogenies (18–20). To test the role of ecological opportunity in driving the morphological component of adaptive radiation more explicitly, Mahler et al. (21) developed a novel approach to model rates of morphological evolution as function of estimated past diversity at nodes of a time-calibrated molecular phylogeny (a similar method can be found in ref. 22). Using estimated lineage diversity as a proxy for past ecological opportunity in island communities of Anolis lizards, they found strong support for diversity dependence of evolutionary rates for body size and limb bone lengths, both of which influence habitat use and performance (21). This result would seem to lend support to a primary role for ecological opportunity in regulating rates of morphological evolution during adaptive radiation. It remains to be tested, however, whether diversity dependence can provide a compelling mechanism to explain patterns of morphological disparity through time in more general contexts, such as on continents, or over longer geological times scales.In this article, I test for diversity dependence of rates of body size and dental evolution in living and fossil members of the dog family, Canidae. Canids are an attractive system for such a study. Living canids exhibit a range of dietary and predatory behaviors that can be readily diagnosed for fossil species on the basis of craniodental traits (23, 24). The canid fossil record is also well sampled, yielding a diverse radiation of ∼140 species (25–27) that spans the Late Eocene (40 Mya) through present day. Perhaps most importantly, however, for the first 35 My of their evolutionary history, canids were restricted to and diversified exclusively within North America. If ecological opportunity plays a prominent role in regulating rates of morphological diversification over geological time scales, we should expect to find support for a link between diversity and the tempo of ecomorphological diversification in continental radiations with excellent fossil records, such as Canidae.     

Evolutionary dynamics of feedback escape and the development of stem-cell-driven cancers

Cancers are thought to arise in tissue stem cells, and similar to healthy tissue, are thought to be maintained by a small population of tumor stem or initiating cells, whereas the majority of tumor cells are more differentiated with limited replicative potential. Healthy tissue homeostasis is achieved by feedback loops, and particular importance has been attached to signals secreted from differentiated cells that inhibit stem-cell division and stem-cell self-renewal, as documented in the olfactory epithelium and other tissues. Therefore, a key event in carcinogenesis must be escape from these feedback loops, which is studied here using evolutionary computational models. We find that out of all potential evolutionary pathways, only one unique sequence of phenotypic transitions can lead to complete escape in stem-cell-driven tumors, even though the required mutations for these transitions are certainly tissue specific. This insight, supported by data, facilitates the search for driver mutations and for therapeutic targets. Different growth patterns can result from feedback escape, which we call "inhibited," "uninhibited," and "sigmoidal," and which are found in published data. The finding of inhibited growth patterns in data indicates that besides architecture, the regulatory mechanisms of healthy tissue continue to operate to a degree in tumors.     

Optimal Design of the Gating and Riser System for Complex Casting Using an Evolutionary Algorithm

The gating and riser system design is essential for both quality and cost in large-scale casting and is expected to reach several objectives simultaneously. However, even with the help of commercial simulation software, the design of gating and riser systems is still the result of a long-term trial-and-error optimal process owing to the conflict between the objectives. Several evolutionary algorithms (EAs) have been reported to be helpful in the selection of the geometrical dimensions of gating and riser systems. In this study, a route with sequential use of a multi-objective EA and single-objective optimization algorithm was developed to help design gating and riser systems, respectively. This route was applied in an actual case and verified using commercial simulation software. The results showed a dramatic decrease in the time cost in design and acceptable casting quality. Thus, the proposed design method is time-saving.     

Repeated climate-linked host shifts have promoted diversification in a temperate clade of leaf-mining flies

A central but little-tested prediction of “escape and radiation” coevolution is that colonization of novel, chemically defended host plant clades accelerates insect herbivore diversification. That theory, in turn, exemplifies one side of a broader debate about the relative influence on clade dynamics of intrinsic (biotic) vs. extrinsic (physical-environmental) forces. Here, we use a fossil-calibrated molecular chronogram to compare the effects of a major biotic factor (repeated shift to a chemically divergent host plant clade) and a major abiotic factor (global climate change) on the macroevolutionary dynamics of a large Cenozoic radiation of phytophagous insects, the leaf-mining fly genus Phytomyza (Diptera: Agromyzidae). We find one of the first statistically supported examples of consistently elevated net diversification accompanying shift to new plant clades. In contrast, we detect no significant direct effect on diversification of major global climate events in the early and late Oligocene. The broader paleoclimatic context strongly suggests, however, that climate change has at times had a strong indirect influence through its effect on the biotic environment. Repeated rapid Miocene radiation of these flies on temperate herbaceous asterids closely corresponds to the dramatic, climate-driven expansion of seasonal, open habitats.     

The emergence and perils of polarization

We provide commentaries on the papers included in the Dynamics of Political Polarization Special Feature. Baldassarri reads the contribution of the papers in light of the theoretical distinction between ideological partisanship, which is generally rooted in sociodemographic and political cleavages, and affective partisanship, which is, instead, mostly fueled by emotional attachment and repulsion, rather than ideology and material interests. The latter, she argues, is likely to lead to a runaway process and threaten the pluralistic bases of contemporary democracy. Page sees the contribution of the many distinct models in the ensemble as potentially contributing more than the parts. Individual papers identify distinct causes of polarization as well as potential solutions. Viewed collectively, the papers suggest that the multiple causes of polarization may self-reinforce, which suggests that successful interventions would require a variety of efforts. Understanding how to construct such interventions may require larger models with greater realism.     

Species invasion progressively disrupts the trophic structure of native food webs

Species invasions can have substantial impacts on native species and ecosystems, with important consequences for biodiversity. How these disturbances drive changes in the trophic structure of native food webs through time is poorly understood. Here, we quantify trophic disruption in freshwater food webs to invasion by an apex fish predator, lake trout, using an extensive stable isotope dataset across a natural gradient of uninvaded and invaded lakes in the northern Rocky Mountains, USA. Lake trout invasion increased fish diet variability (trophic dispersion), displaced native fishes from their reference diets (trophic displacement), and reorganized macroinvertebrate communities, indicating strong food web disruption. Trophic dispersion was greatest 25 to 50 y after colonization and dissipated as food webs stabilized in later stages of invasion (>50 y). For the native apex predator, bull trout, trophic dispersion preceded trophic displacement, leading to their functional loss in late-invasion food webs. Our results demonstrate how invasive species progressively disrupt native food webs via trophic dispersion and displacement, ultimately yielding biological communities strongly divergent from those in uninvaded ecosystems.

Invasive species have caused devastating ecological and economic impacts worldwide (1, 2). For example, invasive species are responsible for the decline of nearly half of the species protected by the US Endangered Species Act and those named on the International Union for Conservation of Nature Red List and cause almost US$120 billion in annual damages in the United States alone (3, 4). The scope of these damages has prompted recent efforts to predict the vulnerability of ecosystems to species invasions and prioritize them for management (5, 6), a process contingent on our ability to understand the mechanisms by which invaders alter food webs through time (7). While the economic harm caused by invasive species is apparent, predicting trophic responses to species invasions remains challenging because complex ecological changes can compound through time (8, 9).Species invasions change interactions within and between communities, with potentially severe consequences for biodiversity and ecosystems (10). Animals adapted to eat diverse foods (i.e., diet generalists) often change their diets to overcome increasing competition for food and/or to avoid new predators following species invasions (11). Those diet changes then manifest in the trophic structure of food webs in two main ways: changing diet variability [i.e., trophic dispersion (12), such as switching from a specialist to a generalist diet] or prey switching [i.e., trophic displacement (13), such as eating insects instead of fish]. Given these patterns, we propose the “trophic disruption hypothesis”: Species cause trophic dispersion and trophic displacement, which, given time, change food web structure and affect biodiversity. Despite some preliminary evidence that these trophic disruptions change as invasion progresses (14, 15), quantitative tests of this hypothesis across a range of intact and invaded ecosystems do not exist.To test the trophic disruption hypothesis, we examined the trophic effects of an invasive piscivorous fish (lake trout; Salvelinus namaycush) across lake food webs in the northern Rocky Mountains, USA. Invasive predatory fishes provide an ideal system to test this hypothesis because they have been widely introduced across the globe and their ability to mediate major changes in the trophic structure of aquatic ecosystems is widely recognized (14). Lake trout have been intentionally, illegally, or invasively established in over 200 waters in western North America (16), resulting in cascading changes within and across ecosystems (17, 18). Populations of bull trout (Salvelinus confluentus), one of the most threatened cold-water fishes in North America, have dramatically declined in most lakes where lake trout have been introduced or invaded (16). Bull trout and lake trout are apex predators and share similar feeding strategies, diets, and morphologies, making competition and predation likely between these species (19). Despite this major conservation threat, no studies have evaluated the impacts of lake trout invasion across entire food webs supporting native bull trout.We leveraged a natural experiment to quantify how trophic dispersion and displacement unfold following species invasion. Though otherwise comparable, our 10 study lakes that contained native bull trout populations ranged in invasion severity from reference (i.e., uninvaded) to fully dominated by lake trout. We used this invasion gradient to simulate the progression of trophic disruption over decades by classifying lakes on a scale of 0 to 1 based on the relative abundance of bull trout to lake trout (reference, 0; midinvasion, 0.4 to 0.8; and late invasion, 0.8 to 1). We used stable nitrogen (N) and carbon (C) isotopes (1,459 samples) to determine how fish diets changed as lake trout invasion progressed. Stable isotope analyses provide time-integrated and energy-based depictions of trophic structure that facilitate understanding food web consequences of species invasions (13). The ratio of stable nitrogen isotopes (¹⁵N:¹⁴N; δ¹⁵N) exhibits stepwise enrichment (often 3 to 4‰) between prey and predators and is used to infer the trophic position of consumers (20). The ratio of stable carbon isotopes (¹³C:¹²C; δ¹³C) varies substantially (>10‰) between littoral-benthic and pelagic primary producers but changes little (often <1‰) from prey to predators and is used to infer energy sources used for secondary production (20). By combining long-term abundance monitoring data and stable isotope analyses, we determined how invasion-induced trophic dispersion and displacement changed over time in these lake food webs.     

Perturbations to trophic interactions and the stability of complex food webs

The pattern of predator–prey interactions is thought to be a key determinant of ecosystem processes and stability. Complex ecological networks are characterized by distributions of interaction strengths that are highly skewed, with many weak and few strong interactors present. Theory suggests that this pattern promotes stability as weak interactors dampen the destabilizing potential of strong interactors. Here, we present an experimental test of this hypothesis and provide empirical evidence that the loss of weak interactors can destabilize communities in nature. We ranked 10 marine consumer species by the strength of their trophic interactions. We removed the strongest and weakest of these interactors from experimental food webs containing >100 species. Extinction of strong interactors produced a dramatic trophic cascade and reduced the temporal stability of key ecosystem process rates, community diversity and resistance to changes in community composition. Loss of weak interactors also proved damaging for our experimental ecosystems, leading to reductions in the temporal and spatial stability of ecosystem process rates, community diversity, and resistance. These results highlight the importance of conserving species to maintain the stabilizing pattern of trophic interactions in nature, even if they are perceived to have weak effects in the system.     

Metacommunity theory explains the emergence of food web complexity

Food webs are highly complex ecological networks, dynamic in both space and time. Metacommunity models are now at the core of unified theories of biodiversity, but to date they have not addressed food web complexity. Here we show that metacommunity theory can explain the emergence of species-rich food webs with complex network topologies. Our analysis shows that network branching in the food web is maximized at intermediate colonization rates and limited dispersal scales, which also leads to concomitant peaks in species diversity. Increased food web complexity and species diversity are made possible by the structural role played by network branches that are supported by omnivore and generalist feeding links. Thus, in contrast to traditional food web theory, which emphasizes the destabilizing effect of omnivory feeding in closed systems, metacommunity theory predicts that these feeding links, which are commonly observed in empirical food webs, play a critical structural role as food webs assemble in space. As this mechanism functions at the metacommunity level, evidence for its operation in nature will be obtained through multiscale surveys of food web structure. Finally, we apply our theory to reveal the effects of habitat destruction on network complexity and metacommunity diversity.     

Herbivore diet breadth mediates the cascading effects of carnivores in food webs

Predicting the impact of carnivores on plants has challenged community and food web ecologists for decades. At the same time, the role of predators in the evolution of herbivore dietary specialization has been an unresolved issue in evolutionary ecology. Here, we integrate these perspectives by testing the role of herbivore diet breadth as a predictor of top-down effects of avian predators on herbivores and plants in a forest food web. Using experimental bird exclosures to study a complex community of trees, caterpillars, and birds, we found a robust positive association between caterpillar diet breadth (phylodiversity of host plants used) and the strength of bird predation across 41 caterpillar and eight tree species. Dietary specialization was associated with increased enemy-free space for both camouflaged (n = 33) and warningly signaled (n = 8) caterpillar species. Furthermore, dietary specialization was associated with increased crypsis (camouflaged species only) and more stereotyped resting poses (camouflaged and warningly signaled species), but was unrelated to caterpillar body size. These dynamics in turn cascaded down to plants: a metaanalysis (n = 15 tree species) showed the beneficial effect of birds on trees (i.e., reduced leaf damage) decreased with the proportion of dietary specialist taxa composing a tree species’ herbivore fauna. We conclude that herbivore diet breadth is a key functional trait underlying the trophic effects of carnivores on both herbivores and plants.Predicting the strength of trophic interactions is a major goal in ecology. Because most natural ecosystems contain numerous coexisting species at each trophic level, achieving this goal necessarily involves the integration of theory in evolutionary, community, and food web ecology. In this context, evolutionary ecology explains how traits of organisms adapt them to a fundamental trade-off between resource acquisition and mortality risk from natural enemies (1, 2); community ecology theory links the many patterns and consequences of species interactions to the diversity of traits of those species (2); and food web ecology subsumes this diversity into patterns of trophic structure and dynamics, such as a trophic cascade (3). The recognition that functional traits of species can drive the indirect positive effect of carnivores on plant biomass [trophic cascades broadly defined (4, 5)] provides important insight into the causes of variation in these dynamics (1, 6). An emerging understanding of the functional traits mediating trophic cascade strength includes traits of herbivores that facilitate predator avoidance (7–10), or provide constitutive (11, 12) or induced resistance to predation (13). These examples identify antipredator traits of herbivores as an important mediator of top-down effects on plants within individual tritrophic food chains. However, the role of antipredator (or other) traits of herbivores is currently unclear because there is little work comparing a sufficient number of species within a community to causally implicate particular traits. Such comparative analysis of functional traits within a community could reveal the effects of herbivore community structure on trophic cascade strength. Herbivore community structure is likely to influence cascading effects (14), especially on plants hosting species-rich herbivore assemblages, such as insect herbivores on woody plants (15, 16).Here, we test the hypothesis that herbivore diet breadth—specifically, the diversity of plant species consumed—is a functional trait that predicts both the strength of top-down effects of predators on herbivores and the strength of trophic cascades. Insect herbivores are notable for their species richness and great variation among species in dietary specialization (17, 18). According to the enemy-free space (EFS) hypothesis, dietary specificity has evolved in response to generalist predators because specialist herbivores can more effectively use their host plants for defense or refuge (i.e., EFS) than can generalist herbivores (19). Antipredator traits associated with dietary specificity in herbivorous insects include sequestration of plant toxins (20, 21), aposematism [warning signals coupled with unpalatability (22, 23)], as well as superior crypsis (19). Therefore, herbivore diet breadth, by serving as a surrogate for this suite of antipredator traits, might succeed in predicting the strength of top-down control. We thus extend the EFS hypothesis to link theory in evolutionary, community, and food web ecology through the prediction that plants with herbivore communities dominated by dietary specialists will experience weak trophic cascades, compared with those dominated by dietary generalists (hereafter the “EFS–cascade hypothesis”).Although past work provides support for the EFS hypothesis, experimental tests have been limited in several regards. Comparative tests using multiple herbivore species in the same community show reduced attack rates by predators on dietary specialist vs. generalist species (e.g., refs. 20 and 22–24). These studies typically do not account for phylogenetic nonindependence among the herbivore taxa studied (but see ref. 21), thus leaving open the possibility that inferences are biased by nonindependent comparisons (25). In addition, all tests of the EFS hypothesis have focused on predatory insects (predatory wasps, ants, and hemipterans), and it is unknown whether dietary specialization provides EFS from generalist vertebrate predators such as insectivorous birds, bats, and lizards; these vertebrates are important consumers of plant-feeding insects and are known to indirectly benefit plants (26–28). Finally, past empirical work has been limited to predation trials in which herbivores are presented to predators divorced from the full context of their host plants or habitat, thus preventing herbivores from fully using their host plant for EFS. Consequently, a more thorough testing of the EFS hypothesis is warranted and necessary before extending its predictive power to the strength of top-down effects on herbivores and plants.Studying a food web of trees, caterpillars, and insectivorous birds, we evaluated the EFS hypothesis by comparing the effects of bird predation on the 41 most abundant dietary specialist and generalist caterpillar species in a single forest ecosystem. Notably, our test of the EFS hypothesis assesses vertebrate predator effects on herbivores in situ, i.e., naturally occurring on plants, accounts for phylogenetic nonindependence of herbivores, and investigates mechanisms of EFS by analyzing associations between antipredator traits and herbivore diet breadth. Finally, we tested the EFS–cascade hypothesis for the first time (to our knowledge), using a metaanalysis to determine whether variation in the diet breadth of caterpillar assemblages among 15 tree species is associated with variation in the indirect effects of birds on plants, while accounting for the phylogenetic nonindependence of plants. Importantly, by including data from a total of eight geographic locations, this analysis expanded the scope of inference beyond a single ecosystem.