Brief Communications: Rapid and Costly Ageing in Wild Male Flies

Ageing (senescence) has never been demonstrated convincingly in any insect in the wild, where mean life-spans are probably much shorter than in the laboratory1, and most evidence for senescence in other wild animals (such as mammals) is limited to their reduced survival with age2. Here we show that ageing is detectable in wild populations of a very short-lived insect, the antler fly (Protopiophila litigata), and causes debilitating and costly effects that force a decline not only in survival probability, but also in the reproductive rate of males. Our findings argue against the possibility of a trade-off between fitness components, whereby survival may decline without senescence if investment in reproduction increases with age3, and indicate that ageing rates are subject to intense selection in the wild. Although theory predicts the evolution of rapid senescence in organisms that experience high extrinsic (age-independent) mortality rates4, it has been suggested that very few individuals in these groups (such as insects or small mammals) survive long enough in the wild to exhibit detectable5,6 senescence. We tested for senescence in a wild population of the antler fly, a small dipteran that breeds exclusively on discarded antlers of moose and deer. The tendency of adult flies to spend their lives on a single antler, as well as the long duration of their mating (2.3 h; reference 7), facilitate the acquisition of field data on mating success and survival. We surveyed mating aggregations on nine moose antlers every 2 h over 72 days, and recorded the presence and mating status (single or coupled) of each of 609 individually marked males8

Exoskeleton ageing and its relation to longevity and fecundity in female Australian leaf insects (Phyllium monteithi)

Senescence is a decline in reproduction and survival rate with advancing age resulting from deterioration of somatic tissues and systems throughout the body. Age-related somatic changes (somatic ageing) have been studied extensively in vertebrates but are less well known in other animals, including insects. Since adult insects have very limited ability to repair their exoskeleton, somatic ageing could involve deterioration and discolouration of the cuticle. We investigated age-related changes in wing pigmentation and abdominal cuticle necrosis in females of the Australian leaf insect Phyllium monteithi. Adult females varied markedly in the extent and pattern of pigmentation on their bodies, and we found that pigment spots on the forewings increased in size with age in most individuals. As females aged, most individuals also exhibited increasing levels of abdominal cuticle necrosis, resulting in the loss of abdominal cuticle along the margin of the abdomen. Neither the extent of pigmentation nor cuticle loss were clearly associated with reduced fecundity or longevity in the protected laboratory environment, but it remains unknown whether these age-related changes have functional implications in the wild. Our results show that the P. monteithi exoskeleton undergoes complex changes with age, with potential implications for functional traits and fitness

Offspring size variation within broods as a bet-hedging strategy in unpredictable environments

Offspring size is strikingly variable within species. Although theory can account for variation in offspring size among mothers, an adaptive explanation for variation within individual broods has proven elusive. Theoretical considerations of this problem assume that producing offspring that are too small results in reduced offspring viability, but producing offspring that are too large (for that environment) results only in a lost opportunity for increased fecundity. However, logic and recent evidence suggest that offspring above a certain size will also have lower fitness, such that mothers face fitness penalties on either side of an optimum. Although theory assuming intermediate optima has been developed for other diversification traits, the implications of this idea for selection on intra-brood variance in offspring size have not been explored theoretically. Here we model the fitness of mothers producing offspring of uniform vs. variable size in unpredictably variable environments and compare these two strategies under a variety of conditions. Our model predicts that producing variably sized offspring results in higher mean maternal fitness and less variation in fitness among generations when there is a maximum and minimum viable offspring size, and many mothers under- or over-estimate this optimum. This effect is especially strong when the viable offspring size range is narrow relative to the range of environmental variation. To determine whether this prediction is consistent with empirical evidence, we compare within- and among-mother variation in offspring size for 5 phyla of marine invertebrates with different developmental modes corresponding to contrasting levels of environmental predictability. Our comparative analysis reveals that in the developmental mode in which mothers are unlikely to anticipate the relationship between offspring size and performance, size-variation within mothers exceeds variation among mothers, but the converse is true when optimal offspring size is likely to be more predictable. Together, our results support the hypothesis that variation in offspring size within broods can reflect an adaptive strategy for dealing with unpredictably variable environments. We suggest that when there is a minimum and a maximum viable offspring size and the environment is unpredictable, selection will act on both the mean and variance of offspring size

Sex effects on life span and senescence in the wild when dates of birth and death are unknown

Males and females allocate and schedule reproductive effort in very different ways. Because the timing and amount of reproductive effort influence survival and thus the optimization of life histories, mortality and senescence are predicted to be sex specific. However, age-specific mortality rates of wild animals are often difficult to quantify in natural populations. Studies that report mortality rates from natural populations are, therefore, almost entirely confined to long-lived, easy-to-track species such as large mammals and birds. Here, we employ a novel approach using capture–mark–recapture data from a wild population of black field crickets (Teleogryllus commodus) to test for sex differences in demographic aging. In this species, the age of captured adults cannot be readily determined, and animals cannot be reliably captured or observed every night, resulting in demographic data on individuals whose dates of birth and death are unknown. We implement a recently developed life-table analysis for wild-caught individuals of unknown age, in combination with a well-established capture–mark–recapture methodology that models probabilistic dates of death. This unified analytical framework makes it possible to test for aging in wild, hard-to track animals. Using these methods to fit Gompertz models of age-specific mortality, we show that male crickets have higher mortality rates throughout life than female crickets. Furthermore, males and females both exhibit increasing mortality rates with age, indicating senescence, but the rate of senescence is not sex specific. Thus, observed sex differences in longevity are probably due to differences in baseline mortality rather than aging. Our findings illustrate the complexity of the relationships between sex, background mortality, and senescence rate in wild populations, showing that the elevated mortality rate of males need not be coupled with an elevated rate of aging

Revisiting telegony:Offspring inherit an acquired characteristic of their mother's previous mate

Newly discovered non-genetic mechanisms break the link between genes and inheritance, thereby also raising the possibility that previous mating partners could influence traits in offspring sired by subsequent males that mate with the same female (‘telegony’). In the fly Telostylinus angusticollis, males transmit their environmentally acquired condition via paternal effects on offspring body size. We manipulated male condition, and mated females to two males in high or low condition in a fully crossed design. Although the second male sired a large majority of offspring, offspring body size was influenced by the condition of the first male. This effect was not observed when females were exposed to the first male without mating, implicating semen-mediated effects rather than female differential allocation based on pre-mating assessment of male quality. Our results reveal a novel type of transgenerational effect with potential implications for the evolution of reproductive strategies

Reappraising Sexual Coevolution and the Sex Roles

Over recent decades, new ideas have radically altered how we see sex and reproduction. The implications of these ideas are still being explored, yielding intriguing discoveries

Parental breeding age effects on descendants' longevity interact over 2 generations in matrilines and patrilines

Individuals within populations vary enormously in mortality risk and longevity, but the causes of this variation remain poorly understood. A potentially important and phylogenetically widespread source of such variation is maternal age at breeding, which typically has negative effects on offspring longevity. Here, we show that paternal age can affect offspring longevity as strongly as maternal age does and that breeding age effects can interact over 2 generations in both matrilines and patrilines. We manipulated maternal and paternal ages at breeding over 2 generations in the neriid fly Telostylinus angusticollis. To determine whether breeding age effects can be modulated by the environment, we also manipulated larval diet and male competitive environment in the first generation. We found separate and interactive effects of parental and grand-parental ages at breeding on descendants' mortality rate and life span in both matrilines and patrilines. These breeding age effects were not modulated by grand-parental larval diet quality or competitive environment. Our findings suggest that variation in maternal and paternal ages at breeding could contribute substantially to intrapopulation variation in mortality and longevity

Cell-Specific “Competition for Calories� Drives Asymmetric Nutrient-Energy Partitioning, Obesity, and Metabolic Diseases in Human and Non-human Animals

The mammalian body is a complex physiologic “ecosystem� in which cells compete for calories (i.e., nutrient-energy). Axiomatically, cell-types with competitive advantages acquire a greater number of consumed calories, and when possible, increase in size and/or number. Thus, it is logical and parsimonious to posit that obesity is the competitive advantages of fat-cells (adipocytes) driving a disproportionate acquisition and storage of nutrient-energy. Accordingly, we introduce two conceptual frameworks. Asymmetric Nutrient-Energy Partitioning describes the context-dependent, cell-specific competition for calories that determines the partitioning of nutrient-energy to oxidation, anabolism, and/or storage; and Effective Caloric Intake which describes the number of calories available to constrain energy-intake via the inhibition of the sensorimotor appetitive cells in the liver and brain that govern ingestive behaviors. Inherent in these frameworks is the independence and dissociation of the energetic demands of metabolism and the neuro-muscular pathways that initiate ingestive behaviors and energy intake. As we demonstrate, if the sensorimotor cells suffer relative caloric deprivation via asymmetric competition from other cell-types (e.g., skeletal muscle- or fat-cells), energy-intake is increased to compensate for both real and merely apparent deficits in energy-homeostasis (i.e., true and false signals, respectively). Thus, we posit that the chronic positive energy balance (i.e., over-nutrition) that leads to obesity and metabolic diseases is engendered by apparent deficits (i.e., false signals) driven by the asymmetric inter-cellular competition for calories and concomitant differential partitioning of nutrient-energy to storage. These frameworks, in concert with our previous theoretic work, the Maternal Resources Hypothesis, provide a parsimonious and rigorous explanation for the rapid rise in the global prevalence of increased body and fat mass, and associated metabolic dysfunctions in humans and other mammals inclusive of companion, domesticated, laboratory, and feral animals

Evolutionary principles and their practical application

Evolutionary principles are now routinely incorporated into medicine and agriculture. Examples include the design of treatments that slow the evolution of resistance by weeds, pests, and pathogens, and the design of breeding programs that maximize crop yield or quality. Evolutionary principles are also increasingly incorporated into conservation biology, natural resource management, and environmental science. Examples include the protection of small and isolated populations from inbreeding depression, the identification of key traits involved in adaptation to climate change, the design of harvesting regimes that minimize unwanted life-history evolution, and the setting of conservation priorities based on populations, species, or communities that harbor the greatest evolutionary diversity and potential. The adoption of evolutionary principles has proceeded somewhat independently in these different fields, even though the underlying fundamental concepts are the same. We explore these fundamental concepts under four main themes: variation, selection, connectivity, and eco-evolutionary dynamics. Within each theme, we present several key evolutionary principles and illustrate their use in addressing applied problems. We hope that the resulting primer of evolutionary concepts and their practical utility helps to advance a unified multidisciplinary field of applied evolutionary biology