Delayed selfing and resource reallocations in relation to mate availability in the freshwater snail Physa acuta

We study the influence of mate availability on the mating behavior of the self-fertile, preferentially outcrossing freshwater snail Physa acuta. Previous optimization theory indicated that mating system interacts with life-history traits to influence the age at first reproduction, providing three testable predictions. First, isolated individuals should reproduce later than individuals with available mates in the expectancy of finding a partner and avoiding the cost of inbreeding. Second, resource reallocation to future fecundity is needed for such reproductive delays to evolve. Third, the reproductive delay can be optimized with respect to life-history traits (e.g., survival, growth) and the mating system (inbreeding depression). Our results largely validate these predictions. First, reproduction is significantly delayed in isolated individuals ("selfers") as compared with individuals frequently exposed to mates ("outcrossers"). Second, delayed reproduction is associated with reallocation to future growth, survival, and fecundity, although fecundity is also affected by the mating system (selfing vs. outcrossing). Third, the reproductive delay found (approximately 2 wk) is consistent with quantitative predictions from optimization models. The delay is largely heritable, which might be partly explained by among-family differences in the amount of inbreeding depression (mating system) but not growth or survival.     

Divergent selection on,but no genetic conflict over,female and male timing and rate of reproduction in a human population

The sexes often have different phenotypic optima for important life-history traits, and because of a largely shared genome this can lead to a conflict over trait expression. In mammals, the obligate costs of reproduction are higher for females, making reproductive timing and rate especially liable to conflict between the sexes. While studies from wild vertebrates support such sexual conflict, it remains unexplored in humans. We used a pedigreed human population from preindustrial Finland to estimate sexual conflict over age at first and last reproduction, reproductive lifespan and reproductive rate. We found that the phenotypic selection gradients differed between the sexes. We next established significant heritabilities in both sexes for all traits. All traits, except reproductive rate, showed strongly positive intersexual genetic correlations and were strongly genetically correlated with fitness in both sexes. Moreover, the genetic correlations with fitness were almost identical in men and women. For reproductive rate, the intersexual correlation and the correlation with fitness were weaker but again similar between the sexes. Thus, in this population, an apparent sexual conflict at the phenotypic level did not reflect an underlying genetic conflict over the studied reproductive traits. These findings emphasize the need for incorporating genetic perspectives into studies of human life-history evolution.     

Migratory costs and the evolution of egg size and number in introduced and indigenous salmon populations

The trade-off between reproductive investment and migration should be an important factor shaping the evolution of life-history traits among populations following their radiation into habitats with different migratory costs and benefits. An experimentally induced difference in migratory rigor for families of chinook salmon (Oncorhynchus tshawytscha), of approximately 86 km and 413 m elevation, exacted a cost to somatic energy reserves (approximately 17% reduction in metabolizable mass) and ovarian investment (13.7% reduction in ovarian mass). This cost was associated with a reduction in egg size and paralleled the phenotypic pattern of divergence between two introduced New Zealand populations of common origin, presently breeding at sites with different migration distances. The genetic pattern of divergence of these same populations, detected under common rearing, was consistent with compensation for migratory costs (the population that migrates farther invested more in ovarian mass), but egg number more than egg size was associated with this evolution. These evolutionary patterns are consistent with what is known of the inheritance of these traits and with trade-offs and constraints favoring initial evolution in offspring number over offspring size. Analysis of egg number-size patterns of other Pacific salmon populations in their native range supported the hypothesis that migration strongly influences patterns of reproductive allocation, favoring a higher ratio of egg number to egg size with greater migration distance.     

The Evolution of Senescence and Post-Reproductive Lifespan in Guppies (Poecilia reticulata)

The study of post-reproductive lifespan has been of interest primarily with regard to the extended post-menopausal lifespan seen in humans. This unusual feature of human demography has been hypothesized to have evolved because of the “grandmother” effect, or the contributions that post-reproductive females make to the fitness of their children and grandchildren. While some correlative analyses of human populations support this hypothesis, few formal, experimental studies have addressed the evolution of post-reproductive lifespan. As part of an ongoing study of life history evolution in guppies, we compared lifespans of individual guppies derived from populations that differ in their extrinsic mortality rates. Some of these populations co-occur with predators that increase mortality rate, whereas other nearby populations above barrier waterfalls are relatively free from predation. Theory predicts that such differences in extrinsic mortality will select for differences in the age at maturity, allocation of resources to reproduction, and patterns of senescence, including reproductive declines. As part of our evaluation of these predictions, we quantified differences among populations in post-reproductive lifespan. We present here the first formal, comparative study of the evolution of post-reproductive lifespan as a component of the evolution of the entire life history. Guppies that evolved with predators and that experienced high extrinsic mortality mature at an earlier age but also have longer lifespans. We divided the lifespan into three non-overlapping components: birth to age at first reproduction, age at first reproduction to age at last reproduction (reproductive lifespan), and age at last reproduction to age at death (post-reproductive lifespan). Guppies from high-predation environments live longer because they have a longer reproductive lifespan, which is the component of the life history that can make a direct contribution to individual fitness. We found no differences among populations in post-reproductive lifespan, which is as predicted since there can be no contribution of this segment of the life history to an individual's fitness. Prior work on the evolution of post-reproductive lifespan has been dominated by speculation and correlative analyses. We show here that this component of the life history is accessible to formal study as part of experiments that quantify the different segments of an individual's life history. Populations of guppies subject to different mortality pressures from predation evolved differences in total lifespan, but not in post-reproductive lifespan. Rather than showing the direct effects of selection characterizing other life-history traits, post-reproductive lifespan in these fish appears to be a random add-on at the end of the life history. These findings support the hypothesis that differences in lifespan evolving in response to selection are confined to the reproductive lifespan, or those segments of the life history that make a direct contribution to fitness. We also show, for the first time, that fish can have reproductive senescence and extended post-reproductive lifespans despite the general observation that they are capable of producing new primary oocytes throughout their lives.     

The evolution of senescence and post-reproductive lifespan in guppies (Poecilia reticulata)

The study of post-reproductive lifespan has been of interest primarily with regard to the extended post-menopausal lifespan seen in humans. This unusual feature of human demography has been hypothesized to have evolved because of the “grandmother” effect, or the contributions that post-reproductive females make to the fitness of their children and grandchildren. While some correlative analyses of human populations support this hypothesis, few formal, experimental studies have addressed the evolution of post-reproductive lifespan. As part of an ongoing study of life history evolution in guppies, we compared lifespans of individual guppies derived from populations that differ in their extrinsic mortality rates. Some of these populations co-occur with predators that increase mortality rate, whereas other nearby populations above barrier waterfalls are relatively free from predation. Theory predicts that such differences in extrinsic mortality will select for differences in the age at maturity, allocation of resources to reproduction, and patterns of senescence, including reproductive declines. As part of our evaluation of these predictions, we quantified differences among populations in post-reproductive lifespan. We present here the first formal, comparative study of the evolution of post-reproductive lifespan as a component of the evolution of the entire life history.

Guppies that evolved with predators and that experienced high extrinsic mortality mature at an earlier age but also have longer lifespans. We divided the lifespan into three non-overlapping components: birth to age at first reproduction, age at first reproduction to age at last reproduction (reproductive lifespan), and age at last reproduction to age at death (post-reproductive lifespan). Guppies from high-predation environments live longer because they have a longer reproductive lifespan, which is the component of the life history that can make a direct contribution to individual fitness. We found no differences among populations in post-reproductive lifespan, which is as predicted since there can be no contribution of this segment of the life history to an individual's fitness.

Prior work on the evolution of post-reproductive lifespan has been dominated by speculation and correlative analyses. We show here that this component of the life history is accessible to formal study as part of experiments that quantify the different segments of an individual's life history. Populations of guppies subject to different mortality pressures from predation evolved differences in total lifespan, but not in post-reproductive lifespan. Rather than showing the direct effects of selection characterizing other life-history traits, post-reproductive lifespan in these fish appears to be a random add-on at the end of the life history. These findings support the hypothesis that differences in lifespan evolving in response to selection are confined to the reproductive lifespan, or those segments of the life history that make a direct contribution to fitness. We also show, for the first time, that fish can have reproductive senescence and extended post-reproductive lifespans despite the general observation that they are capable of producing new primary oocytes throughout their lives.

     

Individual covariation in life-history traits: seeing the trees despite the forest

We investigated the influence of age on survival and breeding rates in a long-lived species Rissa tridactyla using models with individual random effects permitting variation and covariation in fitness components among individuals. Differences in survival or breeding probabilities among individuals are substantial, and there was positive covariation between survival and breeding probability; birds that were more likely to survive were also more likely to breed, given that they survived. The pattern of age-related variation in these rates detected at the individual level differed from that observed at the population level. Our results provided confirmation of what has been suggested by other investigators: within-cohort phenotypic selection can mask senescence. Although this phenomenon has been extensively studied in humans and captive animals, conclusive evidence of the discrepancy between population-level and individual-level patterns of age-related variation in life-history traits is extremely rare in wild animal populations. Evolutionary studies of the influence of age on life-history traits should use approaches differentiating population level from the genuine influence of age: only the latter is relevant to theories of life-history evolution. The development of models permitting access to individual variation in fitness is a promising advance for the study of senescence and evolutionary processes.     

Population divergence along lines of genetic variance and covariance in the invasive plant Lythrum salicaria in eastern North America

Evolution during biological invasion may occur over contemporary timescales, but the rate of evolutionary change may be inhibited by a lack of standing genetic variation for ecologically relevant traits and by fitness trade-offs among them. The extent to which these genetic constraints limit the evolution of local adaptation during biological invasion has rarely been examined. To investigate genetic constraints on life-history traits, we measured standing genetic variance and covariance in 20 populations of the invasive plant purple loosestrife (Lythrum salicaria) sampled along a latitudinal climatic gradient in eastern North America and grown under uniform conditions in a glasshouse. Genetic variances within and among populations were significant for all traits; however, strong intercorrelations among measurements of seedling growth rate, time to reproductive maturity and adult size suggested that fitness trade-offs have constrained population divergence. Evidence to support this hypothesis was obtained from the genetic variance-covariance matrix (G) and the matrix of (co)variance among population means (D), which were 79.8% (95% C.I. 77.7-82.9%) similar. These results suggest that population divergence during invasive spread of L. salicaria in eastern North America has been constrained by strong genetic correlations among life-history traits, despite large amounts of standing genetic variation for individual traits.     

An empirical test of the bet‐hedging polyandry hypothesis: Female red flour beetles avoid extinction via multiple mating

Bet‐hedging via polyandry (spreading the extinction risk of the female''s lineage over multiple males) may explain the evolution of female multiple mating, which is found in a wide range of animal and plant taxa. This hypothesis posits that females can increase their fitness via polyandrous mating when “unsuitable” males (i.e., males causing reproductive failure for various reasons) are frequent in the population and females cannot discriminate such unsuitable mates. Although recent theoretical studies have shown that polyandry can operate as a bet‐hedging strategy, empirical tests are scarce. In the present study, we tested the bet‐hedging polyandry hypothesis by using the red flour beetle Tribolium castaneum. We compared female reproductive success between monandry and polyandry treatments when females mated with males randomly collected from an experimental population, including 20% irradiated (infertile) males. In addition, we evaluated geometric mean fitness across multiple generations as the index of adaptability of bet‐hedging traits. Polyandrous females showed a significantly higher egg hatching rate and higher geometric mean fitness than monandrous females. These results strongly support the bet‐hedging polyandry hypothesis.     

The evolution of parental care in stochastic environments

Parental care is of fundamental importance to understanding reproductive strategies and allocation decisions. Here, we explore how parental care strategies evolve in variable environments. Using a set of life-history trait trade-offs, we explore the relative costs and benefits of parental care in stochastic environments. Specifically, we consider the cases in which environmental variability results in varying adult death rates, egg death rates, reproductive rate and carrying capacity. Using a measure of fitness appropriate for stochastic environments, we find that parental care has the potential to evolve over a wide range of life-history characteristics when the environment is variable. A variable environment that affects adult or egg death rates can either increase or decrease the fitness of care relative to that in a constant environment, depending on the specific costs of care. Variability that affects carrying capacity or adult reproductive rate has negligible effects on the fitness associated with care. Increasing parental care across different life-history stages can increase fitness gains in variable environments. Costly investment in care is expected to affect the overall fitness benefits, the fitness optimum and rate of evolution of parental care. In general, we find that environmental variability, the life-history traits affected by such variability and the specific costs of care interact to determine whether care will be favoured in a variable environment and what levels of care will be selected.     

Alternative life-histories in a socially polymorphic ant

Social organisms vary greatly in the number of breeders per group; yet, the causes and consequences of this variation remain poorly known. Here, we show that variation in social structure is tightly linked with changes in several fundamental life-history traits within one population of ants. Multiple-queen colonies of Formica selysi were much more populous than single-queen ones. They also occurred in areas of higher nest density, had longer colony lifespan, produced smaller queens that presumably disperse less, and invested less in reproductive individuals relative to workers. These multiple changes in life histories are consistent with a shift in the mode of colony foundation and the degree of philopatry of queens. They may also provide various fitness benefits to members of multiple-queen colonies and are likely to play a central role in the evolution and maintenance of polymorphic social structures.     

Dispersal as a source of variation in age-specific reproductive strategies in a wild population of lizards

Dispersal syndromes describe the patterns of covariation of morphological, behavioural, and life-history traits associated with dispersal. Studying dispersal syndromes is critical to understanding the demographic and genetic consequences of movements. Among studies describing the association of life-history traits with dispersal, there is anecdotal evidence suggesting that dispersal syndromes can vary with age. Recent theory also suggests that dispersive and philopatric individuals might have different age-specific reproductive efforts. In a wild population of the common lizard (Zootoca vivipara), we investigated whether dispersive and philopatric individuals have different age-specific reproductive effort, survival, offspring body condition, and offspring sex ratio. Consistent with theoretical predictions, we found that young dispersive females have a higher reproductive effort than young philopatric females. Our results also suggest that the early high investment in reproduction of dispersive females trades-off with an earlier onset of senescence than in philopatric females. We further found that young dispersive females produce smaller offspring in lower body condition than do young philopatric females. Overall, our results provide empirical evidence that dispersive and philopatric individuals have different age-specific life-history traits.     

Mating frequency and inclusive fitness in Drosophila melanogaster

In many species, increased mating frequency reduces maternal survival and reproduction. In order to understand the evolution of mating frequency, we need to determine the consequences of increased mating frequency for offspring. We conducted an experiment in Drosophila melanogaster in which we manipulated the mating frequency of mothers and examined the survival and fecundity of the mothers and their daughters. We found that mothers with the highest mating frequency had accelerated mortality and more rapid reproductive senescence. On average, they had 50% shorter lives and 30% lower lifetime reproductive success (LRS) than did mothers with the lowest mating frequency. However, mothers with the highest mating frequency produced daughters with 28% greater LRS. This finding implies that frequent mating stimulates cross-generational fitness trade-offs such that maternal fitness is reduced while offspring fitness is enhanced. We evaluate these results using a demographic metric of inclusive fitness. We show that the costs and benefits of mating frequency depend on the growth rate of the population. In an inclusive fitness context, there was no evidence that increased mating frequency results in fitness costs for mothers. These results indicate that cross-generational fitness trade-offs have an important role in sexual selection and life-history evolution.     

A COMPARISON OF INBREEDING DEPRESSION IN LIFE-HISTORY AND MORPHOLOGICAL TRAITS IN ANIMALS

The current study tests the hypothesis that life-history traits (closely related to fitness) show greater inbreeding depression than morphological traits (less closely related to fitness). The mean and median slope of the standardized coefficient of inbreeding depression (the slope of the linear relationship between F and the trait value) for life-history and morphological traits were compared. Slopes for life-history traits were higher than those for morphological traits. At F = 0.25 (full-sibling mating), life-history traits experienced a median reduction of 11.8% in trait value, whereas morphological traits showed a depression in trait value of approximately 2.2%.     

Insular shifts and trade-offs in life-history traits in pond frogs in the Zhoushan Archipelago, China

Island and mainland populations of animal species often differ strikingly in life-history traits such as clutch size, egg size, total reproductive effort and body size. However, despite widespread recognition of insular shifts in these life-history traits in birds, mammals and reptiles, there have been no reports of such life-history shifts in amphibians. Furthermore, most studies have focused on one specific life-history trait without explicit consideration of coordinated evolution among these intimately linked life-history traits, and thus the relationships among these traits are poorly studied. Here we provide the first evidence of insular shifts and trade-offs in a coordinated suite of life-history traits for an amphibian species, the pond frog Rana nigromaculata . Life-history data were collected from eight islands in the Zhoushan Archipelago and neighboring mainland China. We found consistent, significant shifts in all life-history traits between mainland and island populations. Island populations had smaller clutch sizes, larger egg sizes, larger female body size and invested less in total reproductive effort than mainland populations. Significant negative relationships were found between egg size and clutch size and between egg size and total reproductive effort among frog populations after controlling for the effects of body size. Therefore, decreased reproductive effort and clutch size, larger egg size and body size in pond frogs on islands were selected through trade-offs as an overall life-history strategy. Our findings contribute to the formation of a broad, repeatable ecological generality for insular shifts in life-history traits across a range of terrestrial vertebrate taxa.     

Bridging Developmental Boundaries: Lifelong Dietary Patterns Modulate Life Histories in a Parthenogenetic Insect

Determining the effects of lifelong intake patterns on performance is challenging for many species, primarily because of methodological constraints. Here, we used a parthenogenetic insect (Carausius morosus) to determine the effects of limited and unlimited food availability across multiple life-history stages. Using a parthenogen allowed us to quantify intake by juvenile and adult females and to evaluate the morphological, physiological, and life-history responses to intake, all without the confounding influences of pair-housing, mating, and male behavior. In our study, growth rate prior to reproductive maturity was positively correlated with both adult and reproductive lifespans but negatively correlated with total lifespan. Food limitation had opposing effects on lifespan depending on when it was imposed, as it protracted development in juveniles but hastened death in adults. Food limitation also constrained reproduction regardless of when food was limited, although decreased fecundity was especially pronounced in individuals that were food-limited as late juveniles and adults. Additional carry-over effects of juvenile food limitation included smaller adult size and decreased body condition at the adult molt, but these effects were largely mitigated in insects that were switched to ad libitum feeding as late juveniles. Our data provide little support for the existence of a trade-off between longevity and fecundity, perhaps because these functions were fueled by different nutrient pools. However, insects that experienced a switch to the limited diet at reproductive maturity seem to have fueled egg production by drawing down body stores, thus providing some evidence for a life-history trade-off. Our results provide important insights into the effects of food limitation and indicate that performance is modulated by intake both within and across life-history stages.     

Best squirrels trade a long life for an early reproduction

Age at primiparity plays a crucial role in population dynamics and life-history evolution. Long-term data on female North American red squirrels were analysed to study the fitness consequences of delaying first reproduction. Early breeders were born earlier, had a higher breeding success and achieved a higher lifetime reproductive success than females who delayed their first reproduction, which suggests a higher quality of early breeders. However, early breeders had similar mass when tagged, and similar number of food caches available at one year of age as late breeders. Nevertheless, we found evidence of survival costs of early primiparity. Early breeders had a lower survival between one and two years of age than late breeders and a lower lifespan. Our study points out that two reproductive tactics co-occurred in this population: a tactic based on early maturity at the cost of a lower survival versus a tactic based on delayed maturity and long lifespan. High quality individuals express the most profitable tactic by breeding early whereas low quality individuals do the best of a bad job by delaying their first reproduction.     

THE EVOLUTION OF MATERNAL INVESTMENT IN LIZARDS: AN EXPERIMENTAL AND COMPARATIVE ANALYSIS OF EGG SIZE AND ITS EFFECTS ON OFFSPRING PERFORMANCE

I used comparative and experimental analysis of egg size in a Sceloporus lizard to examine a fundamental tenet of life-history theory: the presumed trade-offs among offspring number, offspring size, and performance traits related to offspring size that are likely to influence fitness. I analyzed latitudinal and elevational patterns of egg life-history characteristics among populations and experimentally manipulated egg size and hatchling size by removing yolk from the eggs to examine the causal bases of population differences in offspring traits. Mean clutch size among populations increased to the north (seven vs. 12 eggs/clutch, California vs. Washington), whereas egg size decreased (0.65 g vs. 0.40 g). The elevational patterns in southern California paralleled the latitudinal trends. Several offspring life-history traits that are correlated with egg size also varied geographically; these traits included incubation time, hatchling size, growth rate, and hatchling sprint performance. Hatchling viability of experimentally reduced eggs was remarkably high (~70%), even when up to 50% of the yolk was removed. The experimentally reduced eggs and hatchlings demonstrated the degree to which size influences each of the offspring life-history traits considered. Northern eggs hatched sooner, in part because of their small size. Though growth rate is allometrically related to size within each population (i.e., smaller hatchlings grow faster on a mass-specific basis), population differences in growth rate, as measured in the laboratory, are likely to reflect genetic differentiation in the underlying physiology of growth. Moreover, smaller juveniles, because of experimental reduction, had slower sprint speeds than larger juveniles. The slower sprint speed of hatchlings from Washington compared to hatchlings from California is thus largely due to the fact that eggs are smaller in the Washington population. These results provide a basis for interpreting the evolutionary divergence of the suite of traits involved in the evolution of maternal investment per offspring in lizards. For example, evolutionary divergence in some offspring traits functionally related to size (e.g., sprint speed) may be constrained, relative to traits that are determined by other aspects of development or physiology (e.g., growth). I also discuss issues relating to the evolution of maternal investment that could be tested in laboratory and natural populations using experimentally reduced offspring.     

REPRODUCTIVE BEHAVIOR OF FEMALE BUNTINGS: ISOLATING MECHANISMS IN A HYBRIDIZING PAIR OF SPECIES

The plumage characteristics of male Indigo and Lazuli Buntings are distinct, but the two species can learn each other's songs. Populations comprising Indigo, Lazuli and hybrid individuals occur in the Great Plains of North America, and assortative mating has been inferred from morphometric data. We devised a laboratory assay for determining female preferences for visual and vocal characteristics of conspecific and heterospecific males and for mixtures of these characteristics, such as might be encountered in an overlap population. Females of both species gave more copulation-solicitation displays when exposed to conspecific plumage and vocalizations than when exposed to heterospecific plumage and vocalizations. Females gave intermediate and similar responses to the combinations of conspecific plumage with heterospecific vocalizations and heterospecific plumage with conspecific vocalizations. Thus, in the absence of other potentially important variables, female reproductive behavior is consistent with the hypothesis of assortative mating, based upon both vocal and visual traits of the males and caused by female choice in this semispecies pair.     

Resolving the evolution of sterile worker castes: a window on the advantages and disadvantages of monogamy

Many social Hymenoptera species have morphologically sterile worker castes. It is proposed that the evolutionary routes to this obligate sterility must pass through a ‘monogamy window’, because inclusive fitness favours individuals retaining their reproductive totipotency unless they can rear full siblings. Simulated evolution of sterility, however, finds that ‘point of view’ is critically important. Monogamy is facilitating if sterility is expressed altruistically (i.e. workers defer reproduction to queens), but if sterility results from manipulation by mothers or siblings, monogamy may have no effect or lessen the likelihood of sterility. Overall, the model and data from facultatively eusocial bees suggest that eusociality and sterility are more likely to originate through manipulation than by altruism, casting doubt on a mandatory role for monogamy. Simple kin selection paradigms, such as Hamilton''s rule, can also fail to account for significant evolutionary dynamics created by factors, such as population structure, group-level effects or non-random mating patterns. The easy remedy is to always validate apparently insightful predictions from Hamiltonian equations with life-history appropriate genetic models.