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.

Androgen Elevation Accelerates Reproductive Senescence in Three-Spined Stickleback

Costs of reproduction shape the life-history evolution of investment in current and future reproduction and thereby aging. Androgens have been proposed to regulate the physiology governing these investments. Furthermore, androgens are hypothesized to play a central role in carotenoid-dependent sexual signaling, regulating how much carotenoids are diverted to ornamentation and away from somatic maintenance, increasing oxidative stress, and accelerating aging. We investigated these relationships in male three-spined stickleback in which we elevated 11-ketotestosterone and supplied vitamin E, an antioxidant, in a 2 × 2 design. Androgen elevation shortened the time stickleback maintained reproductive activities. We suspect that this effect is caused by 11-ketotestosterone stimulating investment in current reproduction, but we detected no evidence for this in our measurements of reproductive effort: nest building, body composition, and breeding coloration. Carotenoid-dependent coloration was even slightly decreased by 11-ketotestosterone elevation and was left unaffected by vitamin E. Red coloration correlated with life expectancy and reproductive capacity in a quadratic manner, suggesting overinvestment of the individuals exhibiting the reddest bellies. In contrast, blue iris color showed a negative relationship with survival, suggesting physiological costs of producing this aspect of nuptial coloration. In conclusion, our results support the hypothesis that androgens regulate investment in current versus future reproduction, yet the precise mechanisms remain elusive. The quadratic relationships between sexual signal expression and aspects of quality have wider consequences for how we view sexual selection on ornamentation and its relationship with aging.

Building integral projection models with non-independent vital rates

Population dynamics are functions of several demographic processes including survival, reproduction, somatic growth, and maturation. The rates or probabilities for these processes can vary by time, by location, and by individual. These processes can co-vary and interact to varying degrees, e.g., an animal can only reproduce when it is in a particular maturation state. Population dynamics models that treat the processes as independent may yield somewhat biased or imprecise parameter estimates, as well as predictions of population abundances or densities. However, commonly used integral projection models (IPMs) typically assume independence across these demographic processes. We examine several approaches for modelling between process dependence in IPMs, and include cases where the processes co-vary as a function of time (temporal variation), co-vary within each individual (individual heterogeneity), and combinations of these (temporal variation and individual heterogeneity). We compare our methods to conventional IPMs, which treat vital rates independent, using simulations and a case study of Soay sheep (Ovis aries). In particular, our results indicate that correlation between vital rates can moderately affect variability of some population-level statistics. Therefore, including such dependent structures is generally advisable when fitting IPMs to ascertain whether or not such between vital rate dependencies exist, which in turn can have subsequent impact on population management or life-history evolution.

Reproductive Potential Impacts Body Maintenance Parameters and Global DNA Methylation in Honeybee Workers (Apis mellifera L.)

The widely accepted hypothesis in life history evolution about the trade-off between fecundity and longevity is not confirmed by long-living and highly fecund queens in eusocial insects. The fact that the queens and facultatively sterile workers usually arise from genetically identical eggs but differ in DNA methylation makes them a good model for studies on senescence, eusocial evolution, and epigenetics. Therefore, honeybees seem to be especially useful here because of long living rebel-workers (RW) with high reproductive potential recently described. Longevity, ovariole number, nosema tolerance, and global DNA methylation have been assayed in normal workers (NW) versus RW in hives and cages. RW always lived longer than NW and unexpectedly extended longevity of NW when they were together, similarly as the presence of a queen did. RW lived longer despite the fact that they had higher Nosema spore load; surprisingly they became infected more easily but tolerated the infection better. Global DNA methylation increased with age, being lower in RW than in NW. Therefore, RW are queen-like considering global DNA methylation and the link between fecundity, longevity, and body maintenance. Presented features of RW expands possibilities of the use of honeybees as a model for studies on senescence, nosemosis, eusocial evolution, and epigenetics.

Reproductive Effort and Costs

Predictions about life-history evolution are intellectually bereft without a consideration of trade-offs. Benefits derived from making one life-history ‘decision’ are made at a cost of not realizing potential benefits associated with alternative decisions. These trade-offs are the inevitable product of constraints, often driven by an individual’s differential allocation of fixed resources to reproduction versus survival or growth. These allocations prevent multiple positive outcomes from being simultaneously realized. Reproductive effort is the proportion of total energy or resources allocated to all elements of reproduction. Reproductive effort generates reproductive costs. Increases in current reproductive effort reduce future reproductive success by affecting survival, growth, and/or fecundity. The causal mechanisms of these costs can be energetic, ecological, behavioural, or genetic. Evidence for reproductive costs is widespread. Instances where the evidence of costs is equivocal are usually caused by using among-individual correlations to study what is a within-individual phenomenon.

Evolutionary Demography

Evolutionary demography has grown rapidly in recent years, as the biological topics of life history evolution and evolution in population with complex life cycles have benefitted from and contributed to a broader focus on evolutionary biodemography. This chapter provides a critical summary of the central ideas and methods. The authors emphasise theoretical methods, starting with the main ideas that have attracted attention in the field, the assumptions behind these, and efforts to relax those assumptions, and provide a short account of some new directions. The chapter begins with the classic work of Peter Medawar and William Hamilton and discusses the connections, applications, assumptions, and limitations related to their ideas and results, e.g. sensitivity and corresponding elasticity of growth rate on fertility and survival. It highlights extensions to variable environments and the large body of theory around that topic. Next the chapter discusses how these theoretical methods are related to analyses and theories of post-reproductive life, via the general concept of ‘borrowing fitness’. Finally, the chapter discusses nonlinear models of mutation and selection and density-dependent models.

Kinship dynamics: patterns and consequences of changes in local relatedness

Mounting evidence suggests that patterns of local relatedness can change over time in predictable ways, a process termed kinship dynamics. Kinship dynamics may occur at the level of the population or social group, where the mean relatedness across all members of the population or group changes over time, or at the level of the individual, where an individual's relatedness to its local group changes with age. Kinship dynamics are likely to have fundamental consequences for the evolution of social behaviour and life history because they alter the inclusive fitness payoffs to actions taken at different points in time. For instance, growing evidence suggests that individual kinship dynamics have shaped the evolution of menopause and age-specific patterns of helping and harming. To date, however, the consequences of kinship dynamics for social evolution have not been widely explored. Here we review the patterns of kinship dynamics that can occur in natural populations and highlight how taking a kinship dynamics approach has yielded new insights into behaviour and life-history evolution. We discuss areas where analysing kinship dynamics could provide new insight into social evolution, and we outline some of the challenges in predicting and quantifying kinship dynamics in natural populations.