Chad E. Brassil

Senescence: Rapid and costly ageing in wild male flies

Ageing (senescence) has never been demonstrated convincingly in any insect in the wild, where mean lifespans are probably much shorter than in the laboratory, and most evidence for senescence in other wild animals (such as mammals) is limited to their reduced survival with age. 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 age, and indicate that ageing rates are subject to intense selection in the wild.

Environmental Effects on the Expression of Life Span and Aging: An Extreme Contrast between Wild and Captive Cohorts of Telostylinus angusticollis (Diptera: Neriidae)

Most research on life span and aging has been based on captive populations of short‐lived animals; however, we know very little about the expression of these traits in wild populations of such organisms. Because life span and aging are major components of fitness, the extent to which the results of many evolutionary studies in the laboratory can be generalized to natural settings depends on the degree to which the expression of life span and aging differ in natural environments versus laboratory environments and whether such environmental effects interact with phenotypic variation. We investigated life span and aging in Telostylinus angusticollis in the wild while simultaneously estimating these parameters under a range of conditions in a laboratory stock that was recently established from the same wild population. We found that males live less than one‐fifth as long and age at least twice as rapidly in the wild as do their captive counterparts. In contrast, we found no evidence of aging in wild females. These striking sex‐specific differences between captive and wild flies support the emerging view that environment exerts a profound influence on the expression of life span and aging. These findings have important implications for evolutionary gerontology and, more generally, for the interpretation of fitness estimates in captive populations.

Mean time to extinction of a metapopulation with an Allee effect

The incorporation of Allee effects into a simple metapopulation extinction model reveals a large non-linear reduction in mean time to extinction with small changes in an Allee limit. The extent of this reduction is dependent on the level of migration in the metapopulation. With small amounts of migration, small changes in the Allee limit result in large changes in the mean time to extinction. With higher levels of migration, the mean time to extinction is not as sensitive to changes in the Allee limit, becoming more similar to the single population case. The metapopulation modeled here is a set of nine patches, driven to extinction by environmental stochasticity. A generalized Allee effect is incorporated by a modification of the standard logistic model. The sensitivity of the mean time to extinction to small changes in the Allee limit is especially relevant to population viability analysis, which uses estimates of extinction times for management decisions.

Parasite-mediated disruptive selection in a natural Daphnia population

BackgroundA mismatch has emerged between models and data of host-parasite evolution. Theory readily predicts that parasites can promote host diversity through mechanisms such as disruptive selection. Yet, despite these predictions, empirical evidence for parasite-mediated increases in host diversity remains surprisingly scant.ResultsHere, we document parasite-mediated disruptive selection on a natural Daphnia population during a parasite epidemic. The mean susceptibility of clones collected from the population before and after the epidemic did not differ, but clonal variance and broad-sense heritability of post-epidemic clones were significantly greater, indicating disruptive selection and rapid evolution. A maximum likelihood method that we developed for detecting selection on natural populations also suggests disruptive selection during the epidemic: the distribution of susceptibilities in the population shifted from unimodal prior to the epidemic to bimodal after the epidemic. Interestingly, this same bimodal distribution was retained after a generation of sexual reproduction.ConclusionThese results provide rare empirical support for parasite-driven increases in host genetic diversity, and suggest that this increase can occur rapidly.

Reproductive ageing and sexual selection on male body size in a wild population of antler flies (Protopiophila litigata)

Little is known about the importance of trade‐offs between ageing and other life history traits, or the effects of ageing on sexual selection, particularly in wild populations suffering high extrinsic mortality rates. Life history theory suggests that trade‐offs between reproduction and somatic maintenance may constrain individuals with higher initial reproductive rates to deteriorate more rapidly, resulting in reduced sexual selection strength. However, this trade‐off may be masked by increased condition dependence of reproductive effort in older individuals. We tested for this trade‐off in males in a wild population of antler flies (Protopiophila litigata). High mating rate was associated with reduced longevity, as a result of increased short‐term mortality risk or accelerated ageing in traits affecting viability. In contrast, large body size was associated with accelerated ageing in traits affecting mating success, resulting in reduced sexual selection for large body size. Thus, ageing can affect sexual selection and evolution in wild populations.

Dynamics and responses to mortality rates of competing predators undergoing predator-prey cycles.

Two or more competing predators can coexist using a single homogeneous prey species if the system containing all three undergoes internally generated fluctuations in density. However, the dynamics of species that coexist via this mechanism have not been extensively explored. Here, we examine both the nature of the dynamics and the responses of the mean densities of each predator to mortality imposed upon it or its competitor. The analysis of dynamics uncovers several previously undescribed behaviors for this model, including chaotic fluctuations, and long-term transients that differ significantly from the ultimate patterns of fluctuations. The limiting dynamics of the system can be loosely classified as synchronous cycles, asynchronous cycles, and chaotic dynamics. Synchronous cycles are simple limit cycles with highly positively correlated densities of the two predator species. Asynchronous cycles are limit cycles, frequently of complex form, including a significant period during which prey density is nearly constant while one predator gradually, monotonically replaces the other. Chaotic dynamics are aperiodic and generally have intermediate correlations between predator densities. Continuous changes in density-independent mortality rates often lead to abrupt transitions in mean population sizes, and increases in the mortality rate of one predator may decrease the population size of the competing predator. Similarly, increases in the immigration rate of one predator may decrease its own density and increase the density of the other predator. Proportional changes in one predators birth and death rate functions can have significant effects on the dynamics and mean densities of both predator species. All of these responses to environmental change differ from those observed when competitors coexist stably as the result of resource (prey) partitioning. The patterns described here occur in many other competition models in which there are cycles and differences in the linearity of the responses of consumers to their resources.

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.

Rapid Senescence in Pacific Salmon

Any useful evolutionary theory of senescence must be able to explain variation within and among natural populations and species. This requires a careful characterization of age‐specific mortality rates in nature as well as the intrinsic and extrinsic factors that influence these rates. We perform this task for two populations of semelparous Pacific salmon. During the breeding season, estimated daily mortality rates increased from 0 to 0.2–0.5 (depending on the year) over the course of several weeks. Early‐arriving individuals had a later onset and/or a lower rate of senescence in each breeding season, consistent with adaptive expectations based on temporal variation in selection. Interannual variation in senescence was large, in part because of extrinsic factors (e.g., water temperature). Predation rates were higher in Pick Creek sockeye salmon (anadromous Oncorhynchus nerka) than in Meadow Creek kokanee (nonanadromous O. nerka), but in contrast to evolutionary theory, senescence was not more rapid in the former. Interannual variation may have obscured interpopulation divergence in senescence. Pacific salmon are a promising system for further studies on the physiological, evolutionary, and genetic bases of senescence. In particular, we encourage further research to disentangle the relative importance of adaptive and nonadaptive variation in senescence.

Dynamic versus instantaneous models of diet choice.

We investigate the dynamics of a series of two‐prey‐one‐predator models in which the predator exhibits adaptive diet choice based on the different energy contents and/or handling times of the two prey species. The predator is efficient at exploiting its prey and has a saturating functional response; these two features combine to produce sustained population cycles over a wide range of parameter values. Two types of models of behavioral change are compared. In one class of models (“instantaneous choice”), the probability of acceptance of the poorer prey by the predator instantaneously approximates the optimal choice, given current prey densities. In the second class of models (“dynamic choice”), the probability of acceptance of the poorer prey is a dynamic variable, which begins to change in an adaptive direction when prey densities change but which requires a finite amount of time to approach the new optimal behavior. The two types of models frequently predict qualitatively different population dynamics of the three‐species system, with chaotic dynamics and complex cycles being a common outcome only in the dynamic choice models. In dynamic choice models, factors that reduce the rate of behavioral change when the probability of accepting the poorer prey approaches extreme values often produce complex population dynamics. Instantaneous and dynamic models often predict different average population densities and different indirect interactions between prey species. Alternative dynamic models of behavior are analyzed and suggest, first, that instantaneous choice models may be good approximations in some circumstances and, second, that different types of dynamic choice models often lead to significantly different population dynamics. The results suggest possible behavioral mechanisms leading to complex population dynamics and highlight the need for more empirical study of the dynamics of behavioral change.

Can environmental variation generate positive indirect effects in a model of shared predation

Classic models of apparent competition predict negative indirect effects between prey with a shared enemy. If predator per capita growth rates are nonlinear, then endogenously generated periodic cycles are predicted to generate less negative or even positive indirect effects between prey. Here I determine how exogenous mechanisms such as environmental variation could modify indirect effects. I find that exogenous variation can have a broader range of effects on indirect interactions than endogenously generated cycles. Indirect effects are altered by environmental variation even in simple models for which the per capita growth rate of the predator species is a linear function of population densities. Temporal variation that affects the predator attack rate or the conversion efficiency can lead to large increases or decreases in the indirect effects between prey, dependent on how prey populations co‐vary with the environmental variation. Positive indirect effects can occur when the period of environmental variation is close to the natural period of the biological system and shifts in subharmonic resonance occur with the addition of the second prey. Models that include nonlinear numerical responses generally lead to indirect effects that are sensitive to environmental variation in more parameters and across a wider range of frequencies.