When to shed? Patterns and drivers of time to first ecdysis in snakes.

Time from birth or hatching to the first shed (postnatal ecdysis) in snakes ranges from about an hour to several weeks depending upon the species. We assessed patterns in time to postnatal ecdysis in 102 snake species for which we could source appropriate information, covering 2.6% of all extant snake species, and related measures to various biological traits. Reconstruction revealed ancestral time to postnatal ecdysis to be 11 days. Since time to postnatal ecdysis can be shorter or longer than the ancestral state, we argue that there are several competing drivers for time to postnatal ecdysis. A reduced time to postnatal ecdysis has evolved in several lineages, commonly in ambush-foraging, viviparous vipers, while extended time to postnatal ecdysis is associated with oviparous species with maternal care. Of central importance is the impact of postnatal ecdysis on the scent levels of neonates, resulting in a reduction of time to postnatal ecdysis in chemically cryptic species, while the pivotal role of scent in mother-neonate recognition has resulted in the retention or extension of time to postnatal ecdysis. We showed that postnatal ecdysis improves chemical crypsis. The patterns revealed in this study suggest that measures of time to postnatal ecdysis can provide insights into the biology of snakes and be used as an indicator of certain life history traits.

When one phenotype is not enough: divergent evolutionary trajectories govern venom variation in a widespread rattlesnake species.

Understanding the origin and maintenance of phenotypic variation, particularly across a continuous spatial distribution, represents a key challenge in evolutionary biology. For this, animal venoms represent ideal study systems: they are complex, variable, yet easily quantifiable molecular phenotypes with a clear function. Rattlesnakes display tremendous variation in their venom composition, mostly through strongly dichotomous venom strategies, which may even coexist within a single species. Here, through dense, widespread population-level sampling of the Mojave rattlesnake, Crotalus scutulatus, we show that genomic structural variation at multiple loci underlies extreme geographical variation in venom composition, which is maintained despite extensive gene flow. Unexpectedly, neither diet composition nor neutral population structure explain venom variation. Instead, venom divergence is strongly correlated with environmental conditions. Individual toxin genes correlate with distinct environmental factors, suggesting that different selective pressures can act on individual loci independently of their co-expression patterns or genomic proximity. Our results challenge common assumptions about diet composition as the key selective driver of snake venom evolution and emphasize how the interplay between genomic architecture and local-scale spatial heterogeneity in selective pressures may facilitate the retention of adaptive functional polymorphisms across a continuous space.

Seed ingestion and germination in rattlesnakes: overlooked agents of rescue and secondary dispersal.

Seed dispersal is a key evolutionary process and a central theme in the population ecology of terrestrial plants. The primary producers of most land-based ecosystems are propagated by and maintained through various mechanisms of seed dispersal that involve both abiotic and biotic modes of transportation. By far the most common biotic seed transport mechanism is zoochory, whereby seeds, or fruits containing them, are dispersed through the activities of animals. Rodents are one group of mammals that commonly prey on seeds (granivores) and play a critical, often destructive, role in primary dispersal and the dynamics of plant communities. In North America, geomyid, heteromyid and some sciurid rodents have specialized cheek pouches for transporting seeds from plant source to larder, where they are often eliminated from the pool of plant propagules by consumption. These seed-laden rodents are commonly consumed by snakes as they forage, but unlike raptors, coyotes, bobcats, and other endothermic predators which eat rodents and are known or implicated to be secondary seed dispersers, the role of snakes in seed dispersal remains unexplored. Here, using museum-preserved specimens, we show that in nature three desert-dwelling rattlesnake species consumed heteromyids with seeds in their cheek pouches. By examining the entire gut we discovered, furthermore, that secondarily ingested seeds can germinate in rattlesnake colons. In terms of secondary dispersal, rattlesnakes are best described as diplochorous. Because seed rescue and secondary dispersal in snakes has yet to be investigated, and because numerous other snake species consume granivorous and frugivorous birds and mammals, our observations offer direction for further empirical studies of this unusual but potentially important channel for seed dispersal.

Evolutionary Scenarios and Primate Natural History.

Scenarios summarize evolutionary patterns and processes by interpreting organismal traits and their natural history correlates in a phylogenetic context. They are constructed by (1) describing phenotypes (including physiology and behavior), ideally with attention to formative roles of development, experience, and culture; (2) inferring homologies, homoplasies, ancestral character states, and their transformations with phylogenetic analyses; and (3) integrating those components with ecological and other ancillary data. At their best, evolutionary scenarios are factually dense narratives that entail no known falsehoods; their empirical and methodological shortcomings are transparent, they might be rejected based on new discoveries, and their potential ideological pitfalls are flagged for scrutiny. They are exemplified here by homoplastic foraging with percussive tools by humans, chimpanzees, capuchins, and macaques; homoplastic hunting with spears by humans and chimpanzees; and private experiences (e.g., sense of fairness, grief) among diverse animals, the homologous or homoplastic status of which often remains unexplored. Although scenarios are problematic when used to bolster political agendas, if constructed carefully and regarded skeptically, they can synthesize knowledge, inspire research, engender public understanding of evolution, enrich ethical debates, and provide a deeper historical context for conservation, including nature appreciation.

Walking and talking the tree of life: Why and how to teach about biodiversity.

Taxonomic details of diversity are an essential scaffolding for biology education, yet outdated methods for teaching the tree of life (TOL), as implied by textbook content and usage, are still commonly employed. Here, we show that the traditional approach only vaguely represents evolutionary relationships, fails to denote major events in the history of life, and relies heavily on memorizing near-meaningless taxonomic ranks. Conversely, a clade-based strategy-focused on common ancestry, monophyletic groups, and derived functional traits-is explicitly based on Darwin's "descent with modification," provides students with a rational system for organizing the details of biodiversity, and readily lends itself to active learning techniques. We advocate for a phylogenetic classification that mirrors the TOL, a pedagogical format of increasingly complex but always hierarchical presentations, and the adoption of active learning technologies and tactics.

Merging paleobiology with conservation biology to guide the future of terrestrial ecosystems.

Conservation of species and ecosystems is increasingly difficult because anthropogenic impacts are pervasive and accelerating. Under this rapid global change, maximizing conservation success requires a paradigm shift from maintaining ecosystems in idealized past states toward facilitating their adaptive and functional capacities, even as species ebb and flow individually. Developing effective strategies under this new paradigm will require deeper understanding of the long-term dynamics that govern ecosystem persistence and reconciliation of conflicts among approaches to conserving historical versus novel ecosystems. Integrating emerging information from conservation biology, paleobiology, and the Earth sciences is an important step forward on the path to success. Maintaining nature in all its aspects will also entail immediately addressing the overarching threats of growing human population, overconsumption, pollution, and climate change.

Cooperative rescue and predator fatality involving a group-living strepsirrhine, Coquerel's sifaka (Propithecus coquereli), and a Madagascar ground boa (Acrantophis madagascariensis).

The interactions between primates and their snake predators are of interest because snakes have influenced the evolution of primate visual systems and predation has driven the evolution of primate behaviour, including group living. However, there are few accounts of primate-snake interactions in the wild. We report an incident from Northwest Madagascar in which a large female Madagascar ground boa (Acrantophis madagascariensis) captured an adult female Coquerel's sifaka (Propithecus coquereli); upon capture, the prey's group members proceeded to bite and scratch the snake until it released the prey, which survived. However, a broken mandible suffered by the boa during the incident led to its death by starvation 2 months later. Our observations demonstrate that, in addition to improved predator detection and deterrence (i.e., mobbing), active defence against some predators may provide an additional benefit to group living in Coquerel's sifaka, and suggest that predation on group-living primates may be more costly for predators than attacking a solitary species of similar body size.

Cryptic sociality in rattlesnakes (Crotalus horridus) detected by kinship analysis.

Research on social behaviour has largely concentrated on birds and mammals in visually active, cooperatively breeding groups (although such systems are relatively rare) and focused much less on species that rarely interact other than for mating and parental care. We used microsatellite markers to characterize relatedness among aggregations of timber rattlesnakes (Crotalus horridus), a putatively solitary reptile that relies heavily on chemical cues, and found that juveniles and pregnant females preferentially aggregate with kin under certain conditions. The ability to recognize kin and enhance indirect fitness thus might be far more widespread than implied by studies of animals whose behaviour is primarily visually and/or acoustically mediated, and we predict that molecular markers will reveal many additional examples of 'cryptic' sociality.

Hunter-gatherers and other primates as prey, predators, and competitors of snakes.

Relationships between primates and snakes are of widespread interest from anthropological, psychological, and evolutionary perspectives, but surprisingly, little is known about the dangers that serpents have posed to people with prehistoric lifestyles and nonhuman primates. Here, we report ethnographic observations of 120 Philippine Agta Negritos when they were still preliterate hunter-gatherers, among whom 26% of adult males had survived predation attempts by reticulated pythons. Six fatal attacks occurred between 1934 and 1973. Agta ate pythons as well as deer, wild pigs, and monkeys, which are also eaten by pythons, and therefore, the two species were reciprocally prey, predators, and potential competitors. Natural history data document snake predation on tree shrews and 26 species of nonhuman primates as well as many species of primates approaching, mobbing, killing, and sometimes eating snakes. These findings, interpreted within the context of snake and primate phylogenies, corroborate the hypothesis that complex ecological interactions have long characterized our shared evolutionary history.

Territorial behavior in Taiwanese kukrisnakes (Oligodon formosanus).

The independent evolutionary origin of a complex trait, within a lineage otherwise lacking it, provides a powerful opportunity to test hypotheses on selective forces. Territorial defense of an area containing resources (such as food or shelter) is widespread in lizards but not snakes. Our studies on an insular population of Taiwanese kukrisnakes (Oligodon formosanus) show that females of this species actively defend sea turtle nests by repelling conspecifics for long periods (weeks) until the turtle eggs hatch or are consumed. A clutch of turtle eggs comprises a large, long-lasting food resource, unlike the prey types exploited by other types of snakes. Snakes of this species have formidable weaponry (massively enlarged teeth that are used for slitting eggshells), and when threatened, these snakes wave their tails toward the aggressor (an apparent case of head-tail mimicry). Bites to the tail during intraspecific combat bouts thus can have high fitness costs for males (because the hemipenes are housed in the tail). In combination, unusual features of the species (ability to inflict severe damage to male conspecifics) and the local environment (a persistent prey resource, large relative to the snakes consuming it) render resource defense both feasible and advantageous for female kukrisnakes. The (apparently unique) evolution of territorial behavior in this snake species thus provides strong support for the hypothesis that resource defensibility is critical to the evolution of territoriality.

Pleistocene rewilding: an optimistic agenda for twenty-first century conservation.

Large vertebrates are strong interactors in food webs, yet they were lost from most ecosystems after the dispersal of modern humans from Africa and Eurasia. We call for restoration of missing ecological functions and evolutionary potential of lost North American megafauna using extant conspecifics and related taxa. We refer to this restoration as Pleistocene rewilding; it is conceived as carefully managed ecosystem manipulations whereby costs and benefits are objectively addressed on a case-by-case and locality-by-locality basis. Pleistocene rewilding would deliberately promote large, long-lived species over pest and weed assemblages, facilitate the persistence and ecological effectiveness of megafauna on a global scale, and broaden the underlying premise of conservation from managing extinction to encompass restoring ecological and evolutionary processes. Pleistocene rewilding can begin immediately with species such as Bolson tortoises and feral horses and continue through the coming decades with elephants and Holarctic lions. Our exemplar taxa would contribute biological, economic, and cultural benefits to North America. Owners of large tracts of private land in the central and western United States could be the first to implement this restoration. Risks of Pleistocene rewilding include the possibility of altered disease ecology and associated human health implications, as well as unexpected ecological and sociopolitical consequences of reintroductions. Establishment of programs to monitor suites of species interactions and their consequences for biodiversity and ecosystem health will be a significant challenge. Secure fencing would be a major economic cost, and social challenges will include acceptance of predation as an overriding natural process and the incorporation of pre-Columbian ecological frameworks into conservation strategies.

Organisms in nature as a central focus for biology.

Theories summarize science, tell us what to measure when we test hypotheses, and help us study nature better. Nevertheless, organisms themselves embody genetics, development, morphology, physiology and behavior, and they are the units of populations, communities and ecosystems. Biologists seek to understand organisms, their diversification and environmental relationships--not theories and experiments per se--and discoveries of new organisms and new facts about organisms reset the research cycles of hypothesis testing that underlie conceptually progressive science. I argue here that recent disagreements about the fate of natural history are thus more apparent than real and should not distract us from addressing important issues. The conservation of biodiversity requires factual knowledge of particular organisms, yet we know little or nothing about most species, and organismal diversity is often poorly represented in biological education. Accordingly, I urge those who are especially concerned with teaching and conservation to seek increased financial and curricular support for descriptive natural history, which is so fundamental to many of the applied facets of biology.

Predation upon reptiles in Mediterranean habitats of Chile, Spain and California: A comparative analysis.

Pradation on reptiles at three Mediterranean-type habitat sites was assessed by computing the incidence of reptiles as a percentage of vertebrates in the diet of each predator species and the incidence of each reptile species as prey for the entire assemblage of predators at each locality. The overall importance of reptiles is lowest in Chile, intermediate in California, and highest in Spain. These differences do not appear to result from interlocality variation in the size distributions of predators or of prey. The incidence of particular reptile species as prey is correlated with their relative abundances in Spain and California, but not in Chile. Behavioral and morphological attributes evidently make some species more vulnerable to predation and others less so than their abundances would predict. Predation on the speciose lizard genus Liolaemus in Chile is sufficient to promote behavioral responses but not major morphological divergence.

The guild structure of a community of predatory vertebrates in central Chile.

The trophic ecology of eleven predator species (Falconiforms: Buteo polyosoma, Elanus leucurus, Falco sparverius, Geranoaetus melanoleucus, Parabuteo unicinctus; Strigiforms: Athene cunicularia, Bubo virginianus, Tyto alba; Carnivores: Dusicyon culpaeus; Snakes: Philodryas chamissonis, Tachymenis peruviana) in two nearby localities of central Chile is analyzed. The localities exhibit the typical climate (hot-dry summers, coldrainy winters), and vegetation (chaparral), of mediterranean ecosystems. Densities of the staple prey (small mammals) were estimated by seasonal trapping during two years in both open and dense patches of chaparral.The trophic parameters examined are: 1) proportion of diurnal, crepuscular, or nocturnal prey found in the predators' diet; 2) relationship between abundance of different mammalian prey in the predators' diet, and in both open and densely vegetated habitat patches; 3) mean weight and variance of weight of small mammal prey consumed; 4) average weight of the predators; 5) food-niche breadth of the predators; 6) relationship between average weight of predators and mean weight of mammalian prey taken, its variance, and food-niche breadth; 7) overlap in food-niche between all the predator species; 8) guild packing of the predators. Parameters 1) and 2) are used to assess the importance of temporal and habitat segregation of the predators, respectively; parameters 3), 4), 5), and 6) provide information on the possibilities of partitioning the prey resources among the predators; parameters 1), 2), 7) and 8) are used to investigate the organization of the community in terms of guilds.Three niche dimensions seem to be important in determining the structure of the predator community: 1) hunting activity period (diurno-crepuscular, nocturno-crepuscular), 2) hunting habitat (open, or both open and dense patches), and 3) mean prey size taken. Segregation along these three axes results in generally low food niche overlaps (<54% in 47 of the 55 pairwise comparisons) among the predators, but it is not possible to determine whether this was produced by competitive interactions or stochastic differences. Three guilds (niche overlap >90% in pair-wise comparisons) can be recognized: a) the carnivorous-insectivorous guild formed by the diurnal raptors A. cunicularia and F. sparverius, which tend to hunt in open habitat patches; b) the herpetophagous guild formed by the diurnal snakes P. chamissonis and T. peruviana, which presumably hunt in open habitat patches; c) the carnivorous guild (highly specialized in the capture of two rodent species) formed by the diurnal raptors B. polyosoma, G. melanoleucus, P. unicinctus, and the carnivore D. culpaeus, which hunt in open habitat patches. The diurnal raptor E. leucurus is not clearly associated with any guild, and the only two nocturnal raptors in the community (B. virginianus and T. alba) exhibit marked differences in their trophic ecology.