Evolution of reproductive effort in a metapopulation with local extinctions and ecological succession

Abstract Using a metapopulation model, we study how local extinctions, limited population life span, and local demographic disequilibrium affect the evolution of the reproductive effort in a species with overlapping generations but no senescence. We show that in a metapopulation with saturation of all sites and an infinite deme maximal life span (no succession), local extinctions simply constitute an additional source of extrinsic mortality. When either the hypothesis of an infinite deme maximal life span or the saturation hypothesis is relaxed, nontrivial predictions arise. in particular, we find interactions between the evolutionarily stable reproductive effort strategy and the demographic dynamics in the metapopulation. We predict that larger reproductive effort may be selected for in habitats of poorer productivity, contrary to what would be predicted in a single population. Also, we predict that higher dispersal rates should favor selection for lower reproductive efforts. However, metapopulation parameters that favor high dispersal rates also favor larger reproductive efforts. Conflicting selection pressures in the metapopulation also allow maintaining evolutionarily stable polymorphism between a low and high reproductive effort for particular trade-offs between survival and fecundity.     

Age is not just a number—Mathematical model suggests senescence affects how fish populations respond to different fishing regimes

Senescence is often described as an age‐dependent increase in natural mortality (known as actuarial senescence) and an age‐dependent decrease in fecundity (known as reproductive senescence), and its role in nature is still poorly understood. Based on empirical estimates of reproductive and actuarial senescence, we used mathematical simulations to explore how senescence affects the population dynamics of Coregonus albula, a small, schooling salmonid fish. Using an empirically based eco‐evolutionary model, we investigated how the presence or absence of senescence affects the eco‐evolutionary dynamics of a fish population during pristine, intensive harvest, and recovery phases. Our simulation results showed that the presence or absence of senescence affected how the population responded to the selection regime. At an individual level, gillnetting caused a larger decline in asymptotic length when senescence was present, compared to the nonsenescent population, and the opposite occurred when fishing was done by trawling. This change was accompanied by evolution toward younger age at maturity. At the population level, the change in biomass and number of fish in response to different fishery size‐selection patterns depended on the presence or absence of senescence. Since most life‐history and fisheries models ignore senescence, they may be over‐estimating reproductive capacity and under‐estimating natural mortality. Our results highlight the need to understand the combined effects of life‐history characters such as senescence and fisheries selection regime to ensure the successful management of our natural resources.     

Evolution of late-life fecundity in Drosophila melanogaster

Late-life fecundity has been shown to plateau at late ages in Drosophila analogously to late-life mortality rates. In this study, we test an evolutionary theory of late life based on the declining force of natural selection that can explain the occurrence of these late-life plateaus in Drosophila. We also examine the viability of eggs laid by late-age females and test a population genetic mechanism that may be involved in the evolution of late-life fecundity: antagonistic pleiotropy. Together these experiments demonstrate that (i) fecundity plateaus at late ages, (ii) plateaus evolve according to the age at which the force of natural selection acting on fecundity reaches zero, (iii) eggs laid by females in late life are viable and (iv) antagonistic pleiotropy is involved in the evolution of late-life fecundity. This study further supports the evolutionary theory of late life based on the age-specific force of natural selection.     

Evolutionary mechanisms of senescence

This paper reviews theories of the evolution of senescence. The population genetic basis for the decline with age in sensitivity of fitness to changes in survival and fecundity is discussed. It is shown that this creates a presure of selection that disproportionately favors performance early in life. The extent of this bias is greater when there is a high level of extrinsic mortality; this accounts for much the diversity in life-history patterns among different taxa. The implications of quantitative genetic theory for experimental tests of alternative population genetic models of senescence are discussed. In particular, the negative genetic correlations between traits predicted by the antagonistic pleiotropy model may be obscured by positive correlations that are inevitable in a multivariate system, or by the effects of variation due to deleterious mutations. The status of the genetic evidence relevant to these theories is discussed.     

When can a clonal organism escape senescence?

Abstract Some clonal organisms may live for thousands of years and show no signs of senescence, while others consistently die after finite life spans. Using two models, we examined how stage-specific life-history rates of a clone's modules determine whether a genetic individual escapes senescence by replacing old modules with new ones. When the rates of clonal or sexual reproduction and survival of individual modules decline with age, clones are more likely to experience senescence. In addition, the models predict that there is a greater tendency to find senescence in terms of a decline in the rate of sexual reproduction with clone age than in terms of an increase in the probability of clone mortality, unless rates of sexual reproduction increase dramatically with module stage. Using a matrix model modified to represent the clonal lifestyle, we show how a trade-off between sexual and clonal reproduction could result in selection for or against clonal senescence. We also show that, in contrast to unitary organisms, the strength of selection on life-history traits can increase with the age of a clone even in a growing population, countering the evolution of senescence.     

Sexual selection effects on the evolution of senescence

Although the basic theories concerning evolution of senescence have been generally accepted for a half-century, interpretation of this paradigm has been constrained by an over-reliance on mortality as both the cause and the measure of senescence. Consideration of both survival and fecundity as components of reproductive value, and integration of sexual selection theory with senescence theory allows reconciliation of long-standing, as well as recent, discrepancies between data and theory. This approach demonstrates that sexual selection on males in polygynous mating systems can have significant effects on the evolution of senescence that could overshadow the selection effects of mortality rates among such animals.     

Selection on female remating interval is influenced by male sperm competition strategies and ejaculate characteristics

Female remating rate dictates the level of sperm competition in a population, and extensive research has focused on how sperm competition generates selection on male ejaculate allocation. Yet the way ejaculate allocation strategies in turn generate selection on female remating rates, which ultimately influence levels of sperm competition, has received much less consideration despite increasing evidence that both mating itself and ejaculate traits affect multiple components of female fitness. Here, we develop theory to examine how the effects of mating on female fertility, fecundity and mortality interact to generate selection on female remating rate. When males produce more fertile ejaculates, females are selected to mate less frequently, thus decreasing levels of sperm competition. This could in turn favour decreased male ejaculate allocation, which could subsequently lead to higher female remating. When remating simultaneously increases female fecundity and mortality, females are selected to mate more frequently, thus exacerbating sperm competition and favouring male traits that convey a competitive advantage even when harmful to female survival. While intuitive when considered separately, these predictions demonstrate the potential for complex coevolutionary dynamics between male ejaculate expenditure and female remating rate, and the correlated evolution of multiple male and female reproductive traits affecting mating, fertility and fecundity.     

Kin selection, local competition, and reproductive skew

In a spatially structured population, limited dispersal gives rise to local relatedness, potentially favoring indiscriminate helping behavior. However, it also leads to local competition, which reduces the benefits of helping local kin. This tension has become the focus for a growing body of theoretical work. Existing models, however, have focused chiefly on the net impact of limited dispersal on cooperative or competitive effort in a homogeneous population. Here, I extend existing models of kin selection in a group-structured population to allow for asymmetries in expected fecundity and reproductive success among group members. I explore the consequent impact of limited dispersal on the evolution of helping and harming behavior, and on the degree of reproductive inequality or skew. I show that when individuals in a group differ in their expected fecundity, limited dispersal gives rise to kin selection for harming behavior on the part of more fecund individuals, and for helping behavior on the part of less fecund individuals. As a result, philopatry tends to exaggerate differences in reproductive success, and so promotes greater reproductive skew.     

Senescence in relation to latitude and migration in birds

Senescence is the age‐related deterioration of the phenotype, explained by accumulation of mutations, antagonistic pleiotropy, free radicals or other mechanisms. I investigated patterns of actuarial senescence in a sample of 169 species of birds in relation to latitude and migration, by analysing longevity records adjusted for sampling effort, survival rate and body mass. Senescence might decrease at low latitudes because of elevated adult survival rates and generally slow life histories. Alternatively, the rate of senescence might increase at low latitudes because of the greater impact of biological interactions such as parasitism, predation and competition on fitness through differential effects of age‐specific mortality (e.g. because immunologically naïve young individuals and immuno‐senescent old individuals might die more frequently than individuals belonging to intermediate age classes). Bird migration entails extensive exercise twice annually, with migrants spending more time in benign environments with little abiotic mortality than residents, migrants having higher adult survival rate and lower annual fecundity than residents, and migrants suffering more from the consequences of oxidative stress than residents. The rate of senescence increased with latitude, as expected because of slow life histories at low latitudes. Independently, rate of senescence decreased with increasing migration distance. These findings were robust to control for potentially confounding effects of body mass, age of first reproduction and phenotypic similarity among species because of common descent.     

Kin selection and natal dispersal in an age-structured population

We examine the effect of iteroparity on the evolution of dispersal for a species living in a stable but fragmented habitat. We use a kin selection model that incorporates the effects of demographic stochasticity on the local age structure and age-specific genetic identities. We consider two cases: when the juvenile dispersal rate is allowed to change with maternal age and when it is not. In the latter case, we find that the unconditional evolutionarily stable dispersal rate increases when the adult survival rate increases. Two antagonistic forces act upon the evolution of age-specific dispersal rates. First, when the local age structure varies between patches of habitat, the intensity of competition between adults and juveniles in the natal patch is, on average, lower for offspring born to older senescent mothers. This selects for decreasing dispersal with maternal age. Second, offspring born to older parents are on average more related to other juveniles in the same patch and they experience a higher intensity of kin competition, which selects for increasing dispersal with maternal age. We show that the evolutionary outcome results from a balance between these two opposing forces, which depends on the amount of variance in age structure among sub-populations.     

Interspecific competition counteracts negative effects of dispersal on adaptation of an arthropod herbivore to a new host

Dispersal and competition have both been suggested to drive variation in adaptability to a new environment, either positively or negatively. A simultaneous experimental test of both mechanisms is however lacking. Here, we experimentally investigate how population dynamics and local adaptation to a new host plant in a model species, the two‐spotted spider mite (Tetranychus urticae), are affected by dispersal from a stock population (no‐adapted) and competition with an already adapted spider mite species (Tetranychus evansi). For the population dynamics, we find that competition generally reduces population size and increases the risk of population extinction. However, these negative effects are counteracted by dispersal. For local adaptation, the roles of competition and dispersal are reversed. Without competition, dispersal exerts a negative effect on adaptation (measured as fecundity) to a novel host and females receiving the highest number of immigrants performed similarly to the stock population females. By contrast, with competition, adding more immigrants did not result in a lower fecundity. Females from populations with competition receiving the highest number of immigrants had a significantly higher fecundity than females from populations without competition (same dispersal treatment) and than the stock population females. We suggest that by exerting a stronger selection on the adapting populations, competition can counteract the migration load effect of dispersal. Interestingly, adaptation to the new host does not significantly reduce performance on the ancestral host, regardless of dispersal rate or competition. Our results highlight that assessments of how species can adapt to changing conditions need to jointly consider connectivity and the community context.     

BIRTH‐ORDER DIFFERENCES CAN DRIVE NATURAL SELECTION ON AGING

Senescence—the deterioration of survival and reproductive capacity with increasing age—is generally held to be an evolutionary consequence of the declining strength of natural selection with increasing age. The diversity in rates of aging observed in nature suggests that the rate at which age‐specific selection weakens is determined by species‐specific ecological factors. We propose that, in iteroparous species, relationships between parental age, offspring birth order, and environment may affect selection on senescence. Later‐born siblings have, on average, older parents than do first borns. Offspring born to older parents may experience different environments in terms of family support or inherited resources, factors often mediated by competition from siblings. Thus, age‐specific selection on parents may change if the environment produces birth‐order related gradients in reproductive success. We use an age‐and‐stage structured population model to investigate the impact of sibling environmental inequality on the expected evolution of senescence. We show that accelerated senescence evolves when later‐born siblings are likely to experience an environment detrimental to lifetime reproduction. In general, sibling inequality is likely to be of particular importance for the evolution of senescence in species such as humans, where family interactions and resource inheritance have important roles in determining lifetime reproduction.     

The short-term and long-term effects of parental age in the bean weevil (Acanthoscelides obtectus)

We examined the influence of parental age on life history traits of their offspring in the lines of bean weevil that have evolved different rates of senescence. Measurements included preadult traits (egg size, embryonic developmental time, total preadult developmental time, preadult viability) and adult traits (body weight, total realized fecundity of females, first day of egg laying, early fecundity, late fecundity and longevity). The negative parental age effects were observed for all traits except for the early and total realized fecundity. We did not detect statistically significant line×parental age interactions for either preadult- or adult-survival, so offspring survival did not change with parental age after selection for early vs. late reproduction. It seems that selection acting on the quality of offspring produced by parents of different ages has not been responsible for the evolution of senescence in bean weevil. This revised version was published online in August 2006 with corrections to the Cover Date.     

Fitness costs in spatially structured environments

The clustering of individuals that results from limited dispersal is a double‐edged sword: although it allows for local interactions to be mostly among related individuals, it also results in increased local competition. Here I show that, because they mitigate local competition, fitness costs such as reduced fecundity or reduced survival are less costly in spatially structured environments than in nonspatial settings. I first present a simple demographic example to illustrate how spatial structure weakens selection against fitness costs. Then, I illustrate the importance of disentangling the evolution of a trait from the evolution of potential associated costs, using an example taken from a recent study investigating the effect of spatial structure on the evolution of host defense. In this example indeed, the differences between spatial and nonspatial selection gradients are due to differences in the fitness costs, thereby undermining interpretations of the results made in terms of the trait only. This illustrates the need to consider fitness costs as proper traits in both theoretical and empirical studies.     

Evolutionary genetics of aging in Daphnia

Evolutionary theory of aging stipulates that aging is inevitable consequence of low effectiveness of natural selection acting on traits expressed late in the life span of the organisms. Two main hypotheses exist: the neutralist mutation-accumulation theory and selectionist antagonistic pleiotropy theory. Both theories predict the increase of genetic variance with age; the antagonistic pleiotropy theory also predicts negative genetic correlation between fitness related traits in the beginning and in the end of the life span. In order to test these predictions we measured life expectancy and age specific mortality in cohorts of 26 c lones of Daphnia magna extracted from a single cyclic parthenogen population. Simultaneously, fecundity and age to maturity were measured in representatives of the same clones. Log mortality increased linearly with age, with little evidence for leveling off, although some replicate cohorts did show a significant leveling off of mortality. Genetic variance of log mortality was significantly higher in the last quarter of the life span than in earlier time intervals. There was a significant positive genetic correlation between early fecundity and early mortality, but not between early fecundity and late mortality. This indicates that, although there is a trade-off between fecundity and survival, this trade-off is not based on pleiotropy across ages and therefore the data does not support the prediction of antagonistic pleiotropy theory.     

Exaggerated evolution of male armaments via male–male competition

Males usually compete to gain access to prospective mates. Through this male–male competition, superior males have a higher chance of passing on their traits to the next generation of male offspring. One category of male traits is armaments, which are weapons used during competition, for example, the chelae of fiddler crabs and the antlers of deer. One consequence of intrasexual selection is the exaggerated evolution of armaments, which can be limited by trade‐offs, such as trade‐offs with male body size. Here, we formulate a game‐theoretic sexual selection model to explore the exaggerated evolution of armaments through male–male competition. The model is used to determine how competition affects the evolution of an armament that is subject to trade‐offs. Our simulation can be used to support the exaggerated evolution hypothesis, that is, male–male competition escalates the rate of evolution of armaments.     

Within‐species variation in long‐term trajectories of growth,fecundity and mortality in the Collembola Folsomia candida

Senescence – the progressive deterioration of organisms with age – affects many traits of which survival and reproduction are the most commonly studied. Recent comparative studies have revealed a remarkable amount of variation in the patterns of ageing across the tree of life. This between‐species diversity raises many questions about the evolution of senescence and of the shapes of the life‐history age trajectories. Here, we study how the different components of the shapes of these life‐history age trajectories can vary within a single species to shed light on the possible constraints involved in their evolution. To do so, we closely followed in controlled laboratory conditions, and for more than 450 days, the mortality, body length and fecundity of small cohorts of two clonal lineages of the Collembola Folsomia candida. We studied three components of the adult mortality trajectory: the baseline mortality, onset and speed of senescence. We found that they can differ between strains of a single species in such a way that, remarkably, an increased life expectancy is not synonymous with a delayed senescence: the strain that grows bigger has the longest life expectancy but suffers from a precocious senescence. We observed marked differences between the strains in the asymptotic body length and reproductive investment. More generally, our results highlight the importance of finely describing the long‐term trajectories of several life‐history traits in order to better understand how the patterns of senescence have been shaped by natural selection.     

Evolution and spatial structure interact to influence plant–herbivore population and community dynamics

An individual-based model of plant–herbivore interactions was developed to test the potentially interactive effects of explicit space and coevolution on population and community dynamics. Individual plants and herbivores resided in cells on a lattice and carried linked interaction genes. Interaction strength between individual plants and herbivores depended on concordance between these genes (gene-for-gene coevolution). Mating and dispersal among individuals were controlled spatially within variably sized neighbourhoods. Without evolution we observed high-frequency plant–herbivore oscillations (blue spectra) with small individual neighbourhoods, and stochastic fluctuations (white spectra) with large neighbourhoods. Evolution resulted in decreased interaction strength, decreased herbivore-induced plant mortality, increased population sizes, and longer-term fluctuations (reddened spectra). Small herbivore neighbourhoods led to herbivore extinction only with evolution. To explore the increased population size response to evolution we ran simulations without evolution while tuning plant–herbivore interaction strength from high to none. We found that herbivore populations were maximized at intermediate levels of interaction strength that coincided with the interaction strength achieved when the system tuned itself through evolution. Overall, our model shows that the small-scale details of phenotypically variable individual-level interactions, leading to evolutionary dynamics, affect large-scale population and community dynamics.     

DOES INCREASED MORTALITY FAVOR THE EVOLUTION OF MORE RAPID SENESCENCE?

It is widely believed (following the 1957 hypothesis of G. C. Williams) that greater rates of “extrinsic” (age- and condition-independent) mortality favor more rapid senescence. However, a recent analysis of mammalian life tables failed to find a significant correlation between minimum adult mortality rate and the rate of senescence. This article presents a simple theoretical analysis of how extrinsic mortality should affect the rate of senescence (i.e., the rate at which probability of mortality increases with age) under different evolutionary and population dynamical assumptions. If population dynamics are density independent, extrinsic mortality should not alter the senescence rate favored by natural selection. If population growth is density dependent and populations are stable, the effect of extrinsic mortality depends on the age specificity of the density dependence and on whether survival or reproduction (or both) are functions of density. It is possible that higher extrinsic mortality will increase the rate of senescence at all ages, decrease the rate at all ages, or increase it at some ages while decreasing it at others. Williams's hypothesis is most likely to be supported when density dependence acts primarily on fertility and does not differentially decrease the fertilities of older individuals. Patterns contrary to Williams's prediction are possible when density dependence acts primarily on the survival or fertility of later ages or when most variation in mortality rates is due to variation in nonextrinsic mortality.     

Reproductive effort in viscous populations

Abstract.— Here I study a kin selection model of reproductive effort, the allocation of resources to fecundity versus survival, in a patch-structured population. Breeding females remain in the same patch for life. Offspring have costly, partial long-distance dispersal and compete for breeding sites, which become vacant upon the death of previous occupants. The main result is that the evolutionarily stable reproductive effort decreases as offspring dispersal rate increases. The result can be understood as follows: In a well-mixed population with global competition, neither adults nor juveniles compete with relatives, but in a patch-structured population with dispersal restricted to the juvenile phase, juveniles experience relatively less competition with relatives than adults, thus making juveniles relatively more valuable. Because this asymmetry between adults and juveniles decreases with the dispersal rate, so does the evolutionarily stable level of allocation to fecundity.