Evolutionary dynamics in the Anthropocene: Life history and intensity of human contact shape antipredator responses.

Humans profoundly impact landscapes, ecosystems, and animal behavior. In many cases, animals living near humans become tolerant of them and reduce antipredator responses. Yet, we still lack an understanding of the underlying evolutionary dynamics behind these shifts in traits that affect animal survival. Here, we used a phylogenetic meta-analysis to determine how the mean and variability in antipredator responses change as a function of the number of generations spent in contact with humans under 3 different contexts: urbanization, captivity, and domestication. We found that any contact with humans leads to a rapid reduction in mean antipredator responses as expected. Notably, the variance among individuals over time observed a short-term increase followed by a gradual decrease, significant for domesticated animals. This implies that intense human contact immediately releases animals from predation pressure and then imposes strong anthropogenic selection on traits. In addition, our results reveal that the loss of antipredator traits due to urbanization is similar to that of domestication but occurs 3 times more slowly. Furthermore, the rapid disappearance of antipredator traits was associated with 2 main life-history traits: foraging guild and whether the species was solitary or gregarious (i.e., group-living). For domesticated animals, this decrease in antipredator behavior was stronger for herbivores than for omnivores or carnivores and for solitary than for gregarious species. By contrast, the decrease in antipredator traits was stronger for gregarious, urbanized species, although this result is based mostly on birds. Our study offers 2 major insights on evolution in the Anthropocene: (1) changes in traits occur rapidly even under unintentional human "interventions" (i.e., urbanization) and (2) there are similarities between the selection pressures exerted by domestication and by urbanization. In all, such changes could affect animal survival in a predator-rich world, but through understanding evolutionary dynamics, we can better predict when and how exposure to humans modify these fitness-related traits.

Bayesian Estimation of Species Divergence Times Using Correlated Quantitative Characters.

Discrete morphological data have been widely used to study species evolution, but the use of quantitative (or continuous) morphological characters is less common. Here, we implement a Bayesian method to estimate species divergence times using quantitative characters. Quantitative character evolution is modeled using Brownian diffusion with character correlation and character variation within populations. Through simulations, we demonstrate that ignoring the population variation (or population "noise") and the correlation among characters leads to biased estimates of divergence times and rate, especially if the correlation and population noise are high. We apply our new method to the analysis of quantitative characters (cranium landmarks) and molecular data from carnivoran mammals. Our results show that time estimates are affected by whether the correlations and population noise are accounted for or ignored in the analysis. The estimates are also affected by the type of data analyzed, with analyses of morphological characters only, molecular data only, or a combination of both; showing noticeable differences among the time estimates. Rate variation of morphological characters among the carnivoran species appears to be very high, with Bayesian model selection indicating that the independent-rates model fits the morphological data better than the autocorrelated-rates model. We suggest that using morphological continuous characters, together with molecular data, can bring a new perspective to the study of species evolution. Our new model is implemented in the MCMCtree computer program for Bayesian inference of divergence times.

Lineage Diversity and Size Disparity in Musteloidea: Testing Patterns of Adaptive Radiation Using Molecular and Fossil-Based Methods.

Adaptive radiation is hypothesized to be a primary mechanism that drives the remarkable species diversity and morphological disparity across the Tree of Life. Tests for adaptive radiation in extant taxa are traditionally estimated from calibrated molecular phylogenies with little input from extinct taxa. With 85 putative species in 33 genera and over 400 described extinct species, the carnivoran superfamily Musteloidea is a prime candidate to investigate patterns of adaptive radiation using both extant- and fossil-based macroevolutionary methods. The species diversity and equally impressive ecological and phenotypic diversity found across Musteloidea is often attributed to two adaptive radiations coinciding with two major climate events, the Eocene-Oligocene transition and the Mid-Miocene Climate Transition. Here, we compiled a novel time-scaled phylogeny for 88% of extant musteloids and used it as a framework for testing the predictions of adaptive radiation hypotheses with respect to rates of lineage diversification and phenotypic evolution. Contrary to expectations, we found no evidence for rapid bursts of lineage diversification at the origin of Musteloidea, and further analyses of lineage diversification rates using molecular and fossil-based methods did not find associations between rates of lineage diversification and the Eocene-Oligocene transition or Mid-Miocene Climate Transition as previously hypothesized. Rather, we found support for decoupled diversification dynamics driven by increased clade carrying capacity in the branches leading to a subclade of elongate mustelids. Supporting decoupled diversification dynamics between the subclade of elongate mustelids and the ancestral musteloid regime is our finding of increased rates of body length evolution, but not body mass evolution, within the decoupled mustelid subclade. The lack of correspondence in rates of body mass and length evolution suggest that phenotypic evolutionary rates under a single morphological metric, even one as influential as mass, may not capture the evolution of diversity in clades that exhibit elongate body shapes. The discordance in evolutionary rates between body length and body mass along with evidence of decoupled diversification dynamics suggests that body elongation might be an innovation for the exploitation of novel Mid-Miocene resources, resulting in the radiation of some musteloids.

Brain size predicts problem-solving ability in mammalian carnivores.

Despite considerable interest in the forces shaping the relationship between brain size and cognitive abilities, it remains controversial whether larger-brained animals are, indeed, better problem-solvers. Recently, several comparative studies have revealed correlations between brain size and traits thought to require advanced cognitive abilities, such as innovation, behavioral flexibility, invasion success, and self-control. However, the general assumption that animals with larger brains have superior cognitive abilities has been heavily criticized, primarily because of the lack of experimental support for it. Here, we designed an experiment to inquire whether specific neuroanatomical or socioecological measures predict success at solving a novel technical problem among species in the mammalian order Carnivora. We presented puzzle boxes, baited with food and scaled to accommodate body size, to members of 39 carnivore species from nine families housed in multiple North American zoos. We found that species with larger brains relative to their body mass were more successful at opening the boxes. In a subset of species, we also used virtual brain endocasts to measure volumes of four gross brain regions and show that some of these regions improve model prediction of success at opening the boxes when included with total brain size and body mass. Socioecological variables, including measures of social complexity and manual dexterity, failed to predict success at opening the boxes. Our results, thus, fail to support the social brain hypothesis but provide important empirical support for the relationship between relative brain size and the ability to solve this novel technical problem.

Coexistence with Large Carnivores Supported by a Predator-Compensation Program.

Compensation programs are used globally to increase tolerance for and help offset economic loss caused by large carnivores. Compensation program funding comes from a variety of sources, and in Wyoming and Idaho, USA and Alberta, Canada this includes revenue from hunting and fishing license sales. We review the patterns of livestock depredation and compensation costs of Alberta's predator-compensation program, and compare Alberta's program to compensation programs in neighboring Canadian and American jurisdictions. Current compensation costs in Alberta are well below historic levels, but have been rapidly increasing in recent years due to an increase in depredation events coupled with increased cattle prices. That increase has caused push back from Alberta's hunting and fishing community that finances the compensation program, although less than 3.6% of Alberta's license levy dollars are used for predator compensation. Hunting effort in Alberta is highest on the same privately owned lands with livestock depredation problems, suggesting that private lands support habitats for hunted ungulate species as well as carnivores. Although compensation programs do not prevent depredation events themselves, compensation programs effectively can support the maintenance of wildlife habitats on private lands.

[Ticks (Acari, ixodidae) of the North Caucasus: Species diversity, host-parasite relationships].

Biological diversity of ixodid tick fauna of the North Caucasus is analyzed. On the whole, 38 tick species are represented in the fauna of the North Caucasus. Their distribution within the region, biotopic features, and host-parasite relationships of different stages of ontogenesis are considered.

The more, the better: the use of multiple landmark configurations to solve the phylogenetic relationships in musteloids.

Although the use of landmark data to study shape changes along a phylogenetic tree has become a common practice in evolutionary studies, the role of this sort of data for the inference of phylogenetic relationships remains under debate. Theoretical issues aside, the very existence of historical information in landmark data has been challenged, since phylogenetic analyses have often shown little congruence with alternative sources of evidence. However, most analyses conducted in the past were based upon a single landmark configuration, leaving it unsettled whether the incorporation of multiple configurations may improve the rather poor performance of this data source in most previous phylogenetic analyses. In the present study, we present a phylogenetic analysis of landmark data that combines information derived from several skeletal structures to derive a phylogenetic tree for musteloids. The analysis includes nine configurations representing different skeletal structures for 24 species. The resulting tree presents several notable concordances with phylogenetic hypotheses derived from molecular data. In particular, Mephitidae, Procyonidae, and Lutrinae plus the genera Martes, Mustela, Galictis, and Procyon were retrieved as monophyletic. In addition, other groupings were in agreement with molecular phylogenies or presented only minor discordances. Complementary analyses have also indicated that the results improve substantially when an increasing number of landmark configurations are included in the analysis. The results presented here thus highlight the importance of combining information from multiple structures to derive phylogenetic hypotheses from landmark data.

Impact of the terrestrial-aquatic transition on disparity and rates of evolution in the carnivoran skull.

BACKGROUND: Which factors influence the distribution patterns of morphological diversity among clades? The adaptive radiation model predicts that a clade entering new ecological niche will experience high rates of evolution early in its history, followed by a gradual slowing. Here we measure disparity and rates of evolution in Carnivora, specifically focusing on the terrestrial-aquatic transition in Pinnipedia. We analyze fissiped (mostly terrestrial, arboreal, and semi-arboreal, but also including the semi-aquatic otter) and pinniped (secondarily aquatic) carnivorans as a case study of an extreme ecological transition. We used 3D geometric morphometrics to quantify cranial shape in 151 carnivoran specimens (64 fissiped, 87 pinniped) and five exceptionally-preserved fossil pinnipeds, including the stem-pinniped Enaliarctos emlongi. Range-based and variance-based disparity measures were compared between pinnipeds and fissipeds. To distinguish between evolutionary modes, a Brownian motion model was compared to selective regime shifts associated with the terrestrial-aquatic transition and at the base of Pinnipedia. Further, evolutionary patterns were estimated on individual branches using both Ornstein-Uhlenbeck and Independent Evolution models, to examine the origin of pinniped diversity. RESULTS: Pinnipeds exhibit greater cranial disparity than fissipeds, even though they are less taxonomically diverse and, as a clade nested within fissipeds, phylogenetically younger. Despite this, there is no increase in the rate of morphological evolution at the base of Pinnipedia, as would be predicted by an adaptive radiation model, and a Brownian motion model of evolution is supported. Instead basal pinnipeds populated new areas of morphospace via low to moderate rates of evolution in new directions, followed by later bursts within the crown-group, potentially associated with ecological diversification within the marine realm. CONCLUSION: The transition to an aquatic habitat in carnivorans resulted in a shift in cranial morphology without an increase in rate in the stem lineage, contra to the adaptive radiation model. Instead these data suggest a release from evolutionary constraint model, followed by aquatic diversifications within crown families.

Continental faunal exchange and the asymmetrical radiation of carnivores.

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

Carnivorous dinocephalian from the Middle Permian of Brazil and tetrapod dispersal in Pangaea.

The medial Permian (~270-260 Ma: Guadalupian) was a time of important tetrapod faunal changes, in particular reflecting a turnover from pelycosaurian- to therapsid-grade synapsids. Until now, most knowledge on tetrapod distribution during the medial Permian has come from fossils found in the South African Karoo and the Russian Platform, whereas other areas of Pangaea are still poorly known. We present evidence for the presence of a terrestrial carnivorous vertebrate from the Middle Permian of South America based on a complete skull. Pampaphoneus biccai gen. et sp. nov. was a dinocephalian "mammal-like reptile" member of the Anteosauridae, an early therapsid predator clade known only from the Middle Permian of Russia, Kazakhstan, China, and South Africa. The genus is characterized, among other features, by postorbital bosses, short, bulbous postcanines, and strongly recurved canines. Phylogenetic analysis indicates that the Brazilian dinocephalian occupies a middle position within the Anteosauridae, reinforcing the model of a global distribution for therapsids as early as the Guadalupian. The close phylogenetic relationship of the Brazilian species to dinocephalians from South Africa and the Russian Platform suggests a closer faunistic relationship between South America and eastern Europe than previously thought, lending support to a Pangaea B-type continental reconstruction.

A three-dimensional analysis of the morphological evolution and locomotor behaviour of the carnivoran hind limb.

BACKGROUND: The shape of the appendicular bones in mammals usually reflects adaptations towards different locomotor abilities. However, other aspects such as body size and phylogeny also play an important role in shaping bone design.We used 3D landmark-based geometric morphometrics to analyse the shape of the hind limb bones (i.e., femur, tibia, and pelvic girdle bones) of living and extinct terrestrial carnivorans (Mammalia, Carnivora) to quantitatively investigate the influence of body size, phylogeny, and locomotor behaviour in shaping the morphology of these bones. We also investigated the main patterns of morphological variation within a phylogenetic context. RESULTS: Size and phylogeny strongly influence the shape of the hind limb bones. In contrast, adaptations towards different modes of locomotion seem to have little influence. Principal Components Analysis and the study of phylomorphospaces suggest that the main source of variation in bone shape is a gradient of slenderness-robustness. CONCLUSION: The shape of the hind limb bones is strongly influenced by body size and phylogeny, but not to a similar degree by locomotor behaviour. The slender-robust "morphological bipolarity" found in bone shape variability is probably related to a trade-off between maintaining energetic efficiency and withstanding resistance to stresses. The balance involved in this trade-off impedes the evolution of high phenotypic variability. In fact, both morphological extremes (slender/robust) are adaptive in different selective contexts and lead to a convergence in shape among taxa with extremely different ecologies but with similar biomechanical demands. Strikingly, this "one-to-many mapping" pattern of evolution between morphology and ecology in hind limb bones is in complete contrast to the "many-to-one mapping" pattern found in the evolution of carnivoran skull shape. The results suggest that there are more constraints in the evolution of the shape of the appendicular skeleton than in that of skull shape because of the strong biomechanical constraints imposed by terrestrial locomotion.

A dynamic global equilibrium in carnivoran diversification over 20 million years.

The ecological and evolutionary processes leading to present-day biological diversity can be inferred by reconstructing the phylogeny of living organisms, and then modelling potential processes that could have produced this genealogy. A more direct approach is to estimate past processes from the fossil record. The Carnivora (Mammalia) has both substantial extant species richness and a rich fossil record. We compiled species-level data for over 10 000 fossil occurrences of nearly 1400 carnivoran species. Using this compilation, we estimated extinction, speciation and net diversification for carnivorans through the Neogene (22-2 Ma), while simultaneously modelling sampling probability. Our analyses show that caniforms (dogs, bears and relatives) have higher speciation and extinction rates than feliforms (cats, hyenas and relatives), but lower rates of net diversification. We also find that despite continual species turnover, net carnivoran diversification through the Neogene is surprisingly stable, suggesting a saturated adaptive zone, despite restructuring of the physical environment. This result is strikingly different from analyses of carnivoran diversification estimated from extant species alone. Two intervals show elevated diversification rates (13-12 Ma and 4-3 Ma), although the precise causal factors behind the two peaks in carnivoran diversification remain open questions.

Diversity, disparity, and evolutionary rate estimation for unresolved Yule trees.

The branching structure of biological evolution confers statistical dependencies on phenotypic trait values in related organisms. For this reason, comparative macroevolutionary studies usually begin with an inferred phylogeny that describes the evolutionary relationships of the organisms of interest. The probability of the observed trait data can be computed by assuming a model for trait evolution, such as Brownian motion, over the branches of this fixed tree. However, the phylogenetic tree itself contributes statistical uncertainty to estimates of rates of phenotypic evolution, and many comparative evolutionary biologists regard the tree as a nuisance parameter. In this article, we present a framework for analytically integrating over unknown phylogenetic trees in comparative evolutionary studies by assuming that the tree arises from a continuous-time Markov branching model called the Yule process. To do this, we derive a closed-form expression for the distribution of phylogenetic diversity (PD), which is the sum of branch lengths connecting the species in a clade. We then present a generalization of PD which is equivalent to the expected trait disparity in a set of taxa whose evolutionary relationships are generated by a Yule process and whose traits evolve by Brownian motion. We find expressions for the distribution of expected trait disparity under a Yule tree. Given one or more observations of trait disparity in a clade, we perform fast likelihood-based estimation of the Brownian variance for unresolved clades. Our method does not require simulation or a fixed phylogenetic tree. We conclude with a brief example illustrating Brownian rate estimation for 12 families in the mammalian order Carnivora, in which the phylogenetic tree for each family is unresolved.

Phylogenetically related and ecologically similar carnivores harbour similar parasite assemblages.

Most parasites infect multiple hosts, but what factors determine the range of hosts a given parasite can infect? Understanding the broad scale determinants of parasite distributions across host lineages is important for predicting pathogen emergence in new hosts and for estimating pathogen diversity in understudied host species. In this study, we used a new data set on 793 parasite species reported from free-ranging populations of 64 carnivore species to examine the factors that influence parasite sharing between host species. Our results showed that parasites are more commonly shared between phylogenetically related host species pairs. Additionally, host species with higher similarity in biological traits and greater geographic range overlap were also more likely to share parasite species. Of three measures of phylogenetic relatedness considered here, the number divergence events that separated host species pairs most strongly influenced the likelihood of parasite sharing. We also showed that viruses and helminths tend to infect carnivore hosts within more restricted phylogenetic ranges than expected by chance. Overall, our results underscore the importance of host evolutionary history in determining parasite host range, even when simultaneously considering other factors such as host ecology and geographic distribution.

Late Pleistocene carnivores (Carnivora: Mammalia) from a cave sedimentary deposit in northern Brazil.

The Brazilian Quaternary terrestrial Carnivora are represented by the following families: Canidae, Felidae, Ursidae, Procyonidae Mephitidae and Mustelidae. Their recent evolutionary history in South America is associated with the uplift of the Panamanian Isthmus, and which enabled the Great American Biotic Interchange (GABI). Here we present new fossil records of Carnivora found in a cave in Aurora do Tocantins, Tocantins, northern Brazil. A stratigraphical controlled collection in the sedimentary deposit of the studied cave revealed a fossiliferous level where the following Carnivora taxa were present: Panthera onca, Leopardus sp., Galictis cuja, Procyon cancrivorus, Nasua nasua and Arctotherium wingei. Dating by Electron Spinning Resonance indicates that this assemblage was deposited during the Last Glacial Maximum (LGM), at least, 22.000 YBP. The weasel, G. cuja, is currently reported much further south than the record presented here. This may suggest that the environment around the cave was relatively drier during the LGM, with more open vegetation, and more moderate temperatures than the current Brazilian Cerrado.

Evolutionary patterns of cat-like carnivorans unveil drivers of the sabertooth morphology.

The sabertooth morphology stands as a classic case of convergence, manifesting recurrently across various vertebrate groups, prominently within two carnivorans clades: felids and nimravids. Nonetheless, the evolutionary mechanisms driving these recurring phenotypes remain insufficiently understood, lacking a robust phylogenetic and spatiotemporal framework. We reconstruct the tempo and mode of craniomandibular evolution of Felidae and Nimravidae and evaluate the strength of the dichotomy between conical and saber-toothed species, as well as within saber-toothed morphotypes. To do so, we investigate morphological variation, convergence, phenotypic integration, and evolutionary rates, employing a comprehensive dataset of nearly 200 3D models encompassing mandibles and crania from both extinct and extant feline-like carnivorans, spanning their entire evolutionary timeline. Our results reject the hypothesis of a distinctive sabertooth morphology, revealing instead a continuous spectrum of feline-like phenotypes in both the cranium and mandible, with sporadic instances of unequivocal convergence. Disparity peaked at the end of the Miocene and is usually higher in clades containing taxa with extreme sabertoothed adaptations. We show that taxa with saberteeth exhibit a lower degree of craniomandibular integration, allowing to exhibit a greater range of phenotypes. Those same groups usually show a burst of morphological evolutionary rate at the beginning of their evolutionary history. Consequently, we propose that a reduced degree of integration coupled with rapid evolutionary rates emerge as key components in the development of a sabertooth morphology in multiple clades.

A range-wide synthesis and timeline for phylogeographic events in the red fox (Vulpes vulpes).

BACKGROUND: Many boreo-temperate mammals have a Pleistocene fossil record throughout Eurasia and North America, but only few have a contemporary distribution that spans this large area. Examples of Holarctic-distributed carnivores are the brown bear, grey wolf, and red fox, all three ecological generalists with large dispersal capacity and a high adaptive flexibility. While the two former have been examined extensively across their ranges, no phylogeographic study of the red fox has been conducted across its entire Holarctic range. Moreover, no study included samples from central Asia, leaving a large sampling gap in the middle of the Eurasian landmass. RESULTS: Here we provide the first mitochondrial DNA sequence data of red foxes from central Asia (Siberia), and new sequences from several European populations. In a range-wide synthesis of 729 red fox mitochondrial control region sequences, including 677 previously published and 52 newly obtained sequences, this manuscript describes the pattern and timing of major phylogeographic events in red foxes, using a Bayesian coalescence approach with multiple fossil tip and root calibration points. In a 335 bp alignment we found in total 175 unique haplotypes. All newly sequenced individuals belonged to the previously described Holarctic lineage. Our analyses confirmed the presence of three Nearctic- and two Japan-restricted lineages that were formed since the Mid/Late Pleistocene. CONCLUSIONS: The phylogeographic history of red foxes is highly similar to that previously described for grey wolves and brown bears, indicating that climatic fluctuations and habitat changes since the Pleistocene had similar effects on these highly mobile generalist species. All three species originally diversified in Eurasia and later colonized North America and Japan. North American lineages persisted through the last glacial maximum south of the ice sheets, meeting more recent colonizers from Beringia during postglacial expansion into the northern Nearctic. Both brown bears and red foxes colonized Japan's northern island Hokkaido at least three times, all lineages being most closely related to different mainland lineages. Red foxes, grey wolves, and brown bears thus represent an interesting case where species that occupy similar ecological niches also exhibit similar phylogeographic histories.

Incorporating indels as phylogenetic characters: impact for interfamilial relationships within Arctoidea (Mammalia: Carnivora).

Insertion and deletion events (indels) provide a suite of markers with enormous potential for molecular phylogenetics. Using many more indel characters than those in previous studies, we here for the first time address the impact of indel inclusion on the phylogenetic inferences of Arctoidea (Mammalia: Carnivora). Based on 6843 indel characters from 22 nuclear intron loci of 16 species of Arctoidea, our analyses demonstrate that when the indels were not taken into consideration, the monophyly of Ursidae and Pinnipedia tree and the monophyly of Pinnipedia and Musteloidea tree were both recovered, whereas inclusion of indels by using three different indel coding schemes give identical phylogenetic tree topologies supporting the monophyly of Ursidae and Pinnipedia. Our work brings new perspectives on the previously controversial placements among Arctoidea families, and provides another example demonstrating the importance of identifying and incorporating indels in the phylogenetic analyses of introns. In addition, comparison of indel incorporation methods revealed that the three indel coding methods are all advantageous over treating indels as missing data, given that incorporating indels produces consistent results across methods. This is the first report of the impact of different indel coding schemes on phylogenetic reconstruction at the family level in Carnivora, which indicates that indels should be taken into account in the future phylogenetic analyses.

Moving to stay in place: behavioral mechanisms for coexistence of African large carnivores.

Most ecosystems have multiple predator species that not only compete for shared prey, but also pose direct threats to each other. These intraguild interactions are key drivers of carnivore community structure, with ecosystem-wide cascading effects. Yet, behavioral mechanisms for coexistence of multiple carnivore species remain poorly understood. The challenges of studying large, free-ranging carnivores have resulted in mainly coarse-scale examination of behavioral strategies without information about all interacting competitors. We overcame some of these challenges by examining the concurrent fine-scale movement decisions of almost all individuals of four large mammalian carnivore species in a closed terrestrial system. We found that the intensity ofintraguild interactions did not follow a simple hierarchical allometric pattern, because spatial and behavioral tactics of subordinate species changed with threat and resource levels across seasons. Lions (Panthera leo) were generally unrestricted and anchored themselves in areas rich in not only their principal prey, but also, during periods of resource limitation (dry season), rich in the main prey for other carnivores. Because of this, the greatest cost (potential intraguild predation) for subordinate carnivores was spatially coupled with the highest potential benefit of resource acquisition (prey-rich areas), especially in the dry season. Leopard (P. pardus) and cheetah (Acinonyx jubatus) overlapped with the home range of lions but minimized their risk using fine-scaled avoidance behaviors and restricted resource acquisition tactics. The cost of intraguild competition was most apparent for cheetahs, especially during the wet season, as areas with energetically rewarding large prey (wildebeest) were avoided when they overlapped highly with the activity areas of lions. Contrary to expectation, the smallest species (African wild dog, Lycaon pictus) did not avoid only lions, but also used multiple tactics to minimize encountering all other competitors. Intraguild competition thus forced wild dogs into areas with the lowest resource availability year round. Coexistence of multiple carnivore species has typically been explained by dietary niche separation, but our multi-scaled movement results suggest that differences in resource acquisition may instead be a consequence of avoiding intraguild competition. We generate a more realistic representation of hierarchical behavioral interactions that may ultimately drive spatially explicit trophic structures of multi-predator communities.

Patterns and implications of extensive heterochrony in carnivoran cranial suture closure.

Heterochronic changes in the rate or timing of development underpin many evolutionary transformations. In particular, the onset and rate of bone development have been the focus of many studies across large clades. In contrast, the termination of bone growth, as estimated by suture closure, has been studied far less frequently, although a few recent studies have shown this to represent a variable, although poorly understood, aspect of developmental evolution. Here, we examine suture closure patterns across 25 species of carnivoran mammals, ranging from social-insectivores to hypercarnivores, to assess variation in suture closure across taxa, identify heterochronic shifts in a phylogenetic framework and elucidate the relationship between suture closure timing and ecology. Our results show that heterochronic shifts in suture closure are widespread across Carnivora, with several shifts identified for most major clades. Carnivorans differ from patterns identified for other mammalian clades in showing high variability of palatal suture closure, no correlation between size and level of suture closure, and little phylogenetic signal outside of musteloids. Results further suggest a strong influence of feeding ecology on suture closure pattern. Most of the species with high numbers of heterochronic shifts, such as the walrus and the aardwolf, feed on invertebrates, and these taxa also showed high frequency of closure of the mandibular symphysis, a state that is relatively rare among mammals. Overall, caniforms displayed more heterochronic shifts than feliforms, suggesting that evolutionary changes in suture closure may reflect the lower diversity of cranial morphology in feliforms.