Cancer risk across mammals.

Cancer is a ubiquitous disease of metazoans, predicted to disproportionately affect larger, long-lived organisms owing to their greater number of cell divisions, and thus increased probability of somatic mutations1,2. While elevated cancer risk with larger body size and/or longevity has been documented within species3-5, Peto's paradox indicates the apparent lack of such an association among taxa6. Yet, unequivocal empirical evidence for Peto's paradox is lacking, stemming from the difficulty of estimating cancer risk in non-model species. Here we build and analyse a database on cancer-related mortality using data on adult zoo mammals (110,148 individuals, 191 species) and map age-controlled cancer mortality to the mammalian tree of life. We demonstrate the universality and high frequency of oncogenic phenomena in mammals and reveal substantial differences in cancer mortality across major mammalian orders. We show that the phylogenetic distribution of cancer mortality is associated with diet, with carnivorous mammals (especially mammal-consuming ones) facing the highest cancer-related mortality. Moreover, we provide unequivocal evidence for the body size and longevity components of Peto's paradox by showing that cancer mortality risk is largely independent of both body mass and adult life expectancy across species. These results highlight the key role of life-history evolution in shaping cancer resistance and provide major advancements in the quest for natural anticancer defences.

Survival improvements of marine mammals in zoological institutions mirror historical advances in human longevity.

An intense public debate has fuelled governmental bans on marine mammals held in zoological institutions. The debate rests on the assumption that survival in zoological institutions has been and remains lower than in the wild, albeit the scientific evidence in support of this notion is equivocal. Here, we used statistical methods previously applied to assess historical improvements in human lifespan and data on 8864 individuals of four marine mammal species (harbour seal, Phoca vitulina; California sea lion, Zalophus californianus; polar bear, Ursus maritimus; common bottlenose dolphin, Tursiops truncatus) held in zoos from 1829 to 2020. We found that life expectancy increased up to 3.40 times, and first-year mortality declined up to 31%, during the last century in zoos. Moreover, the life expectancy of animals in zoos is currently 1.65-3.55 times longer than their wild counterparts. Like humans, these improvements have occurred concurrently with advances in management practices, crucial for population welfare. Science-based decisions will help effective legislative changes and ensure better implementation of animal care.

Sex differences in adult lifespan and aging rates of mortality across wild mammals.

In human populations, women consistently outlive men, which suggests profound biological foundations for sex differences in survival. Quantifying whether such sex differences are also pervasive in wild mammals is a crucial challenge in both evolutionary biology and biogerontology. Here, we compile demographic data from 134 mammal populations, encompassing 101 species, to show that the female's median lifespan is on average 18.6% longer than that of conspecific males, whereas in humans the female advantage is on average 7.8%. On the contrary, we do not find any consistent sex differences in aging rates. In addition, sex differences in median adult lifespan and aging rates are both highly variable across species. Our analyses suggest that the magnitude of sex differences in mammalian mortality patterns is likely shaped by local environmental conditions in interaction with the sex-specific costs of sexual selection.

Maximizing the potential for living cell banks to contribute to global conservation priorities.

Although cryobanking represents a powerful conservation tool, a lack of standardized information on the species represented in global cryobanks, and inconsistent prioritization of species for future sampling, hinder the conservation potential of cryobanking, resulting in missed conservation opportunities. We analyze the representation of amphibian, bird, mammal, and reptile species within the San Diego Zoo Wildlife Alliance Frozen Zoo® living cell collection (as of April 2019) and implement a qualitative framework for the prioritization of species for future sampling. We use global conservation assessment schemes (including the International Union for Conservation of Nature (IUCN) Red List of Threatened Species™, the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES), the Alliance for Zero Extinction, the EDGE of Existence, and Climate Change Vulnerability), and opportunities for sample acquisition from the global zoo and aquarium community, to identify priority species for cryobanking. We show that 965 species, including 5% of all IUCN Red List "Threatened" amphibians, birds, mammals, and reptiles, were represented in the collection and that sampling from within existing zoo and aquarium collections could increase representation to 16.6% (by sampling an additional 707 "Threatened" species). High-priority species for future cryobanking efforts include the whooping crane (Grus americana), crested ibis (Nipponia nippon), and Siberian crane (Leucogeranus leucogeranus). Each of these species are listed under every conservation assessment scheme and have ex situ populations available for sampling. We also provide species prioritizations based on subsets of these assessment schemes together with sampling opportunities from the global zoo and aquarium community. We highlight the difficulties in obtaining in situ samples, and encourage the formation of a global cryobanking database together with the establishment of new cryobanks in biodiversity-rich regions.

Coevolution of relative brain size and life expectancy in parrots.

Previous studies have demonstrated a correlation between longevity and brain size in a variety of taxa. Little research has been devoted to understanding this link in parrots; yet parrots are well-known for both their exceptionally long lives and cognitive complexity. We employed a large-scale comparative analysis that investigated the influence of brain size and life-history variables on longevity in parrots. Specifically, we addressed two hypotheses for evolutionary drivers of longevity: the cognitivebuffer hypothesis, which proposes that increased cognitive abilities enable longer lifespans, and the expensive brain hypothesis, which holds that increases in lifespan are caused by prolonged developmental time of, and increased parental investment in, large-brained offspring. We estimated life expectancy from detailed zoo records for 133 818 individuals across 244 parrot species. Using a principled Bayesian approach that addresses data uncertainty and imputation of missing values, we found a consistent correlation between relative brain size and life expectancy in parrots. This correlation was best explained by a direct effect of relative brain size. Notably, we found no effects of developmental time, clutch size or age at first reproduction. Our results suggest that selection for enhanced cognitive abilities in parrots has in turn promoted longer lifespans.

Bridging the Research Gap between Live Collections in Zoos and Preserved Collections in Natural History Museums.

Zoos and natural history museums are both collections-based institutions with important missions in biodiversity research and education. Animals in zoos are a repository and living record of the world's biodiversity, whereas natural history museums are a permanent historical record of snapshots of biodiversity in time. Surprisingly, despite significant overlap in institutional missions, formal partnerships between these institution types are infrequent. Life history information, pedigrees, and medical records maintained at zoos should be seen as complementary to historical records of morphology, genetics, and distribution kept at museums. Through examining both institution types, we synthesize the benefits and challenges of cross-institutional exchanges and propose actions to increase the dialog between zoos and museums. With a growing recognition of the importance of collections to the advancement of scientific research and discovery, a transformational impact could be made with long-term investments in connecting the institutions that are caretakers of living and preserved animals.

Data gaps and opportunities for comparative and conservation biology.

Biodiversity loss is a major challenge. Over the past century, the average rate of vertebrate extinction has been about 100-fold higher than the estimated background rate and population declines continue to increase globally. Birth and death rates determine the pace of population increase or decline, thus driving the expansion or extinction of a species. Design of species conservation policies hence depends on demographic data (e.g., for extinction risk assessments or estimation of harvesting quotas). However, an overview of the accessible data, even for better known taxa, is lacking. Here, we present the Demographic Species Knowledge Index, which classifies the available information for 32,144 (97%) of extant described mammals, birds, reptiles, and amphibians. We show that only 1.3% of the tetrapod species have comprehensive information on birth and death rates. We found no demographic measures, not even crude ones such as maximum life span or typical litter/clutch size, for 65% of threatened tetrapods. More field studies are needed; however, some progress can be made by digitalizing existing knowledge, by imputing data from related species with similar life histories, and by using information from captive populations. We show that data from zoos and aquariums in the Species360 network can significantly improve knowledge for an almost eightfold gain. Assessing the landscape of limited demographic knowledge is essential to prioritize ways to fill data gaps. Such information is urgently needed to implement management strategies to conserve at-risk taxa and to discover new unifying concepts and evolutionary relationships across thousands of tetrapod species.

The diversity of population responses to environmental change.

The current extinction and climate change crises pressure us to predict population dynamics with ever-greater accuracy. Although predictions rest on the well-advanced theory of age-structured populations, two key issues remain poorly explored. Specifically, how the age-dependency in demographic rates and the year-to-year interactions between survival and fecundity affect stochastic population growth rates. We use inference, simulations and mathematical derivations to explore how environmental perturbations determine population growth rates for populations with different age-specific demographic rates and when ages are reduced to stages. We find that stage- vs. age-based models can produce markedly divergent stochastic population growth rates. The differences are most pronounced when there are survival-fecundity-trade-offs, which reduce the variance in the population growth rate. Finally, the expected value and variance of the stochastic growth rates of populations with different age-specific demographic rates can diverge to the extent that, while some populations may thrive, others will inevitably go extinct.

The emergence of longevous populations.

The human lifespan has traversed a long evolutionary and historical path, from short-lived primate ancestors to contemporary Japan, Sweden, and other longevity frontrunners. Analyzing this trajectory is crucial for understanding biological and sociocultural processes that determine the span of life. Here we reveal a fundamental regularity. Two straight lines describe the joint rise of life expectancy and lifespan equality: one for primates and the second one over the full range of human experience from average lifespans as low as 2 y during mortality crises to more than 87 y for Japanese women today. Across the primate order and across human populations, the lives of females tend to be longer and less variable than the lives of males, suggesting deep evolutionary roots to the male disadvantage. Our findings cast fresh light on primate evolution and human history, opening directions for research on inequality, sociality, and aging.

Individual heterogeneity determines sex differences in mortality in a monogamous bird with reversed sexual dimorphism.

Sex differences in mortality are pervasive in vertebrates, and usually result in shorter life spans in the larger sex, although the underlying mechanisms are still unclear. On the other hand, differences in frailty among individuals (i.e. individual heterogeneity), can play a major role in shaping demographic trajectories in wild populations. The link between these two processes has seldom been explored. We used Bayesian survival trajectory analysis to study age-specific mortality trajectories in the Eurasian sparrowhawk (Accipiter nisus), a monogamous raptor with reversed sexual size dimorphism. We tested the effect of individual heterogeneity on age-specific mortality, and the extent by which this heterogeneity was determined by average reproductive output and wing length as measures of an individual's frailty. We found that sex differences in age-specific mortality were primarily driven by the differences in individual heterogeneity between the two sexes. Females were more heterogeneous than males in their level of frailty. Thus, a larger number of females with low frailty are able to survive to older ages than males, with life expectancy for the least frail adult females reaching up to 4·23 years, while for the least frail adult males it was of 2·68 years. We found that 50% of this heterogeneity was determined by average reproductive output and wing length in both sexes. For both, individuals with high average reproductive output had also higher chances to survive. However, the effect of wing length was different between the two sexes. While larger females had higher survival, larger males had lower chances to survive. Our results contribute a novel perspective to the ongoing debate about the mechanisms that drive sex differences in vital rates in vertebrates. Although we found that variables that relate to the cost of reproduction and sexual dimorphism are at least partially involved in determining these sex differences, it is through their effect on the level of frailty that they affect age patterns of mortality. Therefore, our results raise the possibility that observed differences in age-specific demographic rates may in fact be driven by differences in individual heterogeneity.

Identifying species likely threatened by international trade on the IUCN Red List can inform CITES trade measures.

Overexploitation is a major threat to biodiversity and international trade in many species is regulated through the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES). However, there is no established method to systematically determine which species are most at risk from international trade to inform potential trade measures under CITES. Here, we develop a mechanism using the International Union for Conservation of Nature's Red List of Threatened Species to identify species that are likely to be threatened by international trade. Of 2,211 such species, CITES includes 59% (1,307 species), leaving two-fifths overlooked and in potential need of international trade regulation. Our results can inform deliberations on potential proposals to revise trade measures for species at CITES Conference of the Parties meetings. We also show that, for taxa with biological resource use documented as a threat, the number of species threatened by local and national use is four times greater than species likely threatened by international trade. To effectively address the overexploitation of species, interventions focused on achieving sustainability in international trade need to be complemented by commensurate measures to ensure that local and national use and trade of wildlife is well-regulated and sustainable.

Slow and negligible senescence among testudines challenges evolutionary theories of senescence.

Is senescence inevitable and universal for all living organisms, as evolutionary theories predict? Although evidence generally supports this hypothesis, it has been proposed that certain species, such as turtles and tortoises, may exhibit slow or even negligible senescence-i.e., avoiding the increasing risk of death from gradual deterioration with age. In an extensive comparative study of turtles and tortoises living in zoos and aquariums, we show that ~75% of 52 species exhibit slow or negligible senescence. For ~80% of species, aging rates are lower than those in modern humans. We find that body weight positively relates to adult life expectancy in both sexes, and sexual size dimorphism explains sex differences in longevity. Unlike humans and other species, we show that turtles and tortoises may reduce senescence in response to improvements in environmental conditions.

What's left in the tank? Identification of non-ascribed aquarium's coral collections with DNA barcodes as part of an integrated diagnostic approach.

The unprecedented threats to coral reef ecosystems from global climate change require an urgent response from the aquarium community, which is becoming an increasingly vital coral conservation resource. Unfortunately, many hermatypic corals in aquaria are not identified to species level, which hinders assessment of their conservation significance. Traditional methods of species identification using morphology can be challenging, especially to non-taxonomists. DNA barcoding is an option for species identification of Scleractinian corals, especially when used in concert with morphology-based assessment. This study uses DNA barcodes to try to identify aquarium specimens of the diverse reef-forming genus Acropora from 127 samples. We identified to our best current knowledge, to species name 44% of the analysed samples and provided provisional identification for 80% of them (101/127, in the form of a list of species names with associate confidence values). We highlighted a sampling bias in public nucleotide sequences repertories (e.g. GenBank) towards more charismatic and more studied species, even inside a well-studied genus like Acropora. In addition, we showed a potential "single observer" effect with over a quarter of the reference sequences used for these identifications coming from the same study. We propose the use of barcoding and query matching as an additional tool for taxonomic experts and general aquarists, as an additional tool to increase their chances of making high confidence species-level identifications. We produce a standardised and easily repeatable methodology to increase the capacity of aquariums and other facilities to assess non-ascribed species, emphasising the value of integrating this approach with morphological identification optimising usage of authoritative identification guides and expert opinion. Supplementary Information: The online version contains supplementary material available at 10.1007/s12686-021-01250-3.

Economics, life history and international trade data for seven turtle species in Indonesian and Malaysian farms.

We collected data on the trade of seven turtle and tortoise species endemic to Indonesia and Malaysia (Amyda cartilaginea, Batagur borneoensis, Cuora amboinensis, Carettochelys insculpta, Heosemys annandalii, Heosemys grandis, and Heosemys spinosa). The data on those species included: operations costs of three breeding farms and one export facility; species life-history traits; and species international legal trade and confiscation data. We collected data for the facilities (one in Malaysia and three in Indonesia) using site visits and a semi-structured questionnaire. We conducted a literature review to compile relevant information on species' life-history traits to estimate breeding viability. We downloaded species-specific data on international trade from the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) Trade Database for the exporting countries (Malaysia and Indonesia) for 2000-2015. We compared legal trade with confiscation data obtained from CITES. The data in this article can provide insights into the operations of turtle breeding farms in Southeast Asia. These data can be used as a reference for the inspection of breeding farms and for legislative bodies to determine whether captive breeding for select turtle species is feasible.

A standardized dataset for conservation prioritization of songbirds to support CITES.

In this article we present a standardized dataset on 6659 songbirds (Passeriformes) highlighting information relevant to species conservation prioritization with a main focus to support the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES). Data were collected from both scientific and grey literature as well as several online databases. The data are structured into six knowledge categories: Conventions and Treaties, Human Use, Extinction Risk, Management Opportunities, Biological Information, and Intrinsic Values. The Conventions and Treaties category includes the listings for two international conventions, CITES and the Convention on the Conservation of Migratory Species of Wild Animals (CMS), as well as EU listings for the EU Wildlife Trade Regulations and the EU Birds Directive. The Human Use category contains information on both regulated trade collected from the CITES Trade Database and the United States' Law Enforcement Management Information System (LEMIS), and highly aggregated data on seizures which we obtained from TRAFFIC, the United Nations Office on Drugs and Crime (UNODC) and two data sources on traditional medicine. We also present, for the first time, the complete Songbirds in Trade Database (SiTDB), a trade database curated by taxon expert S. Bruslund based on expert knowledge, literature review, market surveys and sale announcements. Data on the types of human use, including traditional medicine are also provided. The knowledge area on Extinction Risk contains data on the species' IUCN Red List status, the Alliance for Zero Extinction Trigger Species status, site and population at the site, the species' IUCN Climate Change Vulnerability Assessment, and the listing of priority species at the Asian Songbird Crisis Summit. In the Management Opportunities category, we gathered data on ex-situ management from Species360 zoo holdings as well as species management plans from the European and North American Zoo Associations (EAZA and AZA, respectively). Biological Information includes data on body mass, clutch size, diet, availability of data from the IUCN Red List on habitat systems, extent of occurrence, generation length, migration pattern, distribution, and biological data from the Demographic Species Knowledge Index, number of occurrences recorded by the Global Biodiversity Information Facility (GBIF) as well as genomic data from the Bird 10 000K Genomes (B10K) project, Vertebrate Genome Project (VGP) and GenBank. Information on invasive species is also part of this knowledge area. The Intrinsic Value category refers to two measures of the species' intrinsic value, namely Ecological and Evolutionary Distinctiveness. In order to make these knowledge areas comparable, we standardized data following the taxonomy of the Handbook of the Birds of the World and Birdlife (Version 4, 2019). The data enable a broad spectrum of analyses and will be useful to scientists for further research and to policymakers, zoos and other conservation stakeholders for future prioritization decisions.

The long lives of primates and the 'invariant rate of ageing' hypothesis.

Is it possible to slow the rate of ageing, or do biological constraints limit its plasticity? We test the 'invariant rate of ageing' hypothesis, which posits that the rate of ageing is relatively fixed within species, with a collection of 39 human and nonhuman primate datasets across seven genera. We first recapitulate, in nonhuman primates, the highly regular relationship between life expectancy and lifespan equality seen in humans. We next demonstrate that variation in the rate of ageing within genera is orders of magnitude smaller than variation in pre-adult and age-independent mortality. Finally, we demonstrate that changes in the rate of ageing, but not other mortality parameters, produce striking, species-atypical changes in mortality patterns. Our results support the invariant rate of ageing hypothesis, implying biological constraints on how much the human rate of ageing can be slowed.

A system wide approach to managing zoo collections for visitor attendance and in situ conservation.

Zoos contribute substantial resources to in situ conservation projects in natural habitats using revenue from visitor attendance, as well as other sources. We use a global dataset of over 450 zoos to develop a model of how zoo composition and socio-economic factors directly and indirectly influence visitor attendance and in situ project activity. We find that zoos with many animals, large animals, high species richness (particularly of mammals), and which are dissimilar to other zoos achieve higher numbers of visitors and contribute to more in situ conservation projects. However, the model strongly supports a trade-off between number of animals and body mass indicating that alternative composition strategies, such as having many small animals, may also be effective. The evidence-base presented here can be used to help guide collection planning processes and increase the in situ contributions from zoos, helping to reduce global biodiversity loss.

Standardized data to support conservation prioritization for sharks and batoids (Elasmobranchii).

We collated and synthesized information on 1,226 Elasmobranch species (i.e., sharks, rays, and skates) globally from a wide range of sources. We obtained curated and standardized data from online databases, legal documents, press releases, and websites. All data were standardized according to the taxonomic nomenclature described in the Catalogue of Life. We grouped data into five categories: 1) biological information, 2) conservation status, 3) management opportunities, 4) use, and 5) inclusion in international conventions and treaties. For species biological information, we included migration, habitat, species characteristics such as length & body weight, their threat to humans, life-history trait data availability from FishBase, whether the species was listed on the Global Register of Migratory Species, the presence of occurrence data from the Global Biodiversity Information Facility (GBIF), information on genomics from GenBank, and species evolutionary distinctiveness scores. For conservation status, we recorded threat status from the International Union for Conservation of Nature Red List of Threatened Species™ and inclusion in the Alliance for Zero Extinction (AZE). For management opportunities, we identified species under human care in zoos and aquariums in the Species360 network, species under management in studbooks from the European Association of Zoos and Aquaria (EAZA), the American Association for Zoos and Aquariums (AZA), and the Zoo and Aquarium Association Australasia (ZAA), as well as data on recovery, management, and action plans at the class, family, and species levels. For use, we collated species-level data on international trade levels from the CITES (the Convention on International Trade in Endangered Species of Wild Fauna and Flora) Trade Database, as used in aquaculture, as bait, and as gamefish, recording the purpose of the trade according to the IUCN Red List and the global catches reported to the FAO (Food and Agriculture Organization of the United Nations). Finally, we collated information from seven international conventions and treaties: CITES, UNCLOS (the United Nations Convention for the Law of the Sea), CMS (the Convention on the Conservation of Migratory Species of Wild Animals), Shark MoU (the Memorandum of Understanding on the Conservation of Migratory Sharks), BERN (the Convention on the Conservation of European Wildlife and Natural Habitats), OSPAR (Protecting and conserving the North-East Atlantic and its resources), and the Barcelona Convention for the Protection of the Marine Environment and the Coastal Region of the Mediterranean. Our data are comparable across databases and will assist further research on in-situ and ex-situ population management for sharks and batoids. Our data can be of use to international policy makers, aquarium curators, management authorities, conservation practitioners, and scientists interested in prioritizing Elasmobranchs for conservation.

Publisher Correction: Open Science principles for accelerating trait-based science across the Tree of Life.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.