Lifetime Reproductive Fitness Research Articles

The heritability of fitness in a wild annual plant population with hierarchical size structure.

The relative magnitude of additive genetic versus residual variation for fitness traits is important in models for predicting the rate of evolution and population persistence in response to changes in the environment. In many annual plants, lifetime reproductive fitness is correlated with end-of-season plant biomass, which can vary significantly from plant to plant in the same population. We measured end-of-season plant biomasses and obtained SNP genotypes of plants in a dense, natural population of the annual plant species Impatiens capensis with hierarchical size structure. These data were used to estimate the amount of heritable variation for position in the size hierarchy and for plant biomass. Additive genetic variance for position in the size hierarchy and plant biomass were both significantly different from zero. These results are discussed in relationship to theory for the heritability of fitness in natural populations and ecological factors that potentially influence heritable variation for fitness in this species.

Benefits of genetic rescue of a critically endangered subspecies from another subspecies outweigh risks: Results of captive breeding trials

Small, isolated populations risk extinction through inbreeding depression, chance loss of beneficial variation, and reduced adaptability to changing environments. Genetic rescue via gene flow from genetically diverse sources is the most effective way to improve fitness of such populations. However, when the only potential source of immigrants is a different subspecies that diverged long ago and occupies a different environment, genetic rescue may lead to reduced fitness of admixed offspring through outbreeding depression or maladaptation. Test cases are needed to evaluate how to manage such potentially risky rescues to deliver enhanced population fitness. The helmeted honeyeater Lichenostomus melanops cassidix is a critically endangered subspecies of the yellow-tufted honeyeater. The sole remaining natural wild population experiences strong inbreeding depression for lifetime reproductive fitness. Captive genetic rescue trials are underway using a neighbouring subspecies, gippslandicus, which diverged from cassidix thousands of years ago and differs in morphology, mobility and preferred habitat. We evaluated short-term reproductive fitness for captive cassidix-cassidix pairs, first- and second-generation intersubspecific crosses and backcrosses to cassidix, while accounting for breeding season, sex, age at breeding, and wild/captive origin of each bird. Most admixed pair-types more readily engaged in breeding, raised more nestlings per nest, and had less male-biased chick sex-ratios than did cassidix-cassidix pairs, with negligible evidence of outbreeding depression. Continuing monitoring of fitness after releases into the wild is recommended, to ensure local adaptation is retained. With potentially riskier rescue increasingly becoming the only option for many populations, our study provides an encouraging test case.

Effects of parental drought on offspring fitness vary among populations of a crop wild relative.

Transgenerational plasticity is a form of non-genetic inheritance that can reduce or enhance offspring fitness depending on parental stress. Yet, the adaptive value of such parental environmental effects and whether their expression varies among populations remain largely unknown. We used self-fertilized lines from climatically distinct populations of the crop wild relative Lupinus angustifolius. In the parental generation, full-siblings were grown in two contrasting watering environments. Then, to robustly separate the within-generation and transgenerational response to drought, we reciprocally assigned the offspring of parents to the same experimental treatments. We measured key functional traits and assessed lifetime reproductive fitness. Offspring of drought-stressed parents produced less reproductive biomass, but a similar number of lighter seeds, in dry soil compared to offspring of genetically identical, well-watered parents, an effect not mediated by differences in seed provisioning. Importantly, while the offspring of parents grown in the favourable environment responded to drought by slightly increasing individual seed mass, the pattern of plasticity of the offspring of drought-grown parents showed the opposite direction, and the negative effects of parental drought on seed mass were more pronounced in populations from cooler and moist habitats. Overall, our results show that parental effects may override immediate adaptive responses to drought and provide evidence of population-level variation in the expression of transgenerational plasticity.

An Evolutionary Model of "Sexual Conflict" Over Women's Age at Marriage: Implications for Child Mortality and Undernutrition.

BackgroundEarly women's marriage is associated with adverse outcomes for mothers and their offspring, including reduced human capital and increased child undernutrition and mortality. Despite preventive efforts, it remains common in many populations and is often favored by cultural norms. A key question is why it remains common, given such penalties. Using an evolutionary perspective, a simple mathematical model was developed to explore women's optimal marriage age under different circumstances, if the sole aim were to maximize maternal or paternal lifetime reproductive fitness (surviving offspring).MethodsThe model was based on several assumptions, supported by empirical evidence, regarding relationships between women's marital age and parental and offspring outcomes. It assumes that later marriage promotes women's autonomy, enhancing control over fertility and childcare, but increases paternity uncertainty. Given these assumptions, optimal marriage ages for maximizing maternal and paternal fitness were calculated. The basic model was then used to simulate environmental changes or public health interventions, including shifts in child mortality, suppression of women's autonomy, or promoting women's contraception or education.ResultsIn the basic model, paternal fitness is maximized at lower women's marriage age than is maternal fitness, with the paternal optimum worsening child undernutrition and mortality. A family planning intervention delays marriage age and reduces child mortality and undernutrition, at a cost to paternal but not maternal fitness. Reductions in child mortality favor earlier marriage but increase child undernutrition, whereas ecological shocks that increase child mortality favor later marriage but reduce fitness of both parents. An education intervention favors later marriage and reduces child mortality and undernutrition, but at a cost to paternal fitness. Efforts to suppress maternal autonomy substantially increase fitness of both parents, but only if other members of the household provide compensatory childcare.ConclusionEarly women's marriage maximizes paternal fitness despite relatively high child mortality and undernutrition, by increasing fertility and reducing paternity uncertainty. This tension between the sexes over the optimal marriage age is sensitive to ecological stresses or interventions. Education interventions seem most likely to improve maternal and child outcomes, but may be resisted by males and their kin as they may reduce paternal fitness.

Resource relocations in relation to dispersal in Tetranychus ludeni Zacher

Life history strategies of a species may affect its invasion success. Here, we used a haplodiploid pest, Tetranychus ludeni Zacher (Acari: Tetranychidae), which is native to Europe but now cosmopolitan, to investigate its life history strategies in relation to its dispersal tendency and distance. We tested whether and how dispersal influenced survival, lifetime fecundity, age-specific reproduction, and life table parameters of mated females. We show that mated females did not trade off their survival and lifetime reproductive output with dispersal but adjusted their resource allocations during different reproductive stages depending on whether and how far they dispersed. Long-distance dispersers invested more in dispersal in their early life while resident mites and short-distance dispersers invested more in reproduction during their early life. These resource allocation strategies may allow long-distance dispersers to explore the novel environment more effectively without compromising lifetime reproductive fitness, contributing to the invasion success of T. ludeni.

Two mouse lines selected for large litter size display different lifetime fecundities.

We recently described two outbred mouse lines that were selected for large litter size at first delivery. However, lifetime fecundity appears to be economically more important for the husbandry of many polytocous species for which mouse lines might serve as bona fide animal models (e.g. for pigs). In the present study, we compared the lifetime fecundities of two highly fertile mouse lines (FL1 and FL2: >20 offspring/litter at first delivery) with those of an unselected control line (ctrl) and two lines that were selected for high body weight (DU6) and high protein mass (DU6P) without selection pressure on fertility. We tested the hypothesis that selection for large litter size at first parturition would also increase lifetime fecundity in mice, and we observed very large differences between lines. Whereas FL1 and ctrl delivered up to nine and ten litters, none of the DU6 and DU6P females gave birth to more than five litters. In line with this observation, FL1 delivered the most pups per lifetime (85.7/female). FL2 females produced the largest average litter sizes (20.4 pups/litter) in the first four litters; however, they displayed a reduced number of litters. With the exception of ctrl, litter sizes declined from litter to litter. Repeated delivery of litters with high offspring numbers did not affect the general health of FL females. The presented data demonstrate that two biodiverse, highly fertile mouse lines selected for large litter size at first delivery show different lifetime reproductive fitness levels. Thus, these mouse lines might serve as valuable mouse models for investigating lifetime productivity and longevity in farm animals.

High rates of consecutive spawning and precise homing in Sakhalin taimen (Parahucho perryi)

The frequency of reproduction and homing success are crucial in determining the lifetime reproductive fitness of iteroparous salmonids. We examined consecutive spawning and homing by Sakhalin taimen (Parahucho perryi), one of the least-studied iteroparous salmonids. The average consecutive return rate was 69.5%, the highest ever reported for an iteroparous salmonid. The consecutive return rates were highest for large spawners, females, and individuals with active inter-tributary movements in the preceding year. We estimated tributary-scale repeat homing rates to be 50–87%, which was significantly higher than expected by chance alone. The repeat homing rates were higher for spawners that entered tributaries with more abundant spawners in the preceding year, which is consistent with the pheromone hypothesis because the abundance of spawners in a tributary is expected to correlate to the concentration of chemical homing cues emanating from offspring in the following year. These extremely high consecutive return and homing rates likely facilitated local adaptation over evolutionary time scales and have contributed to population stability in this river system. These same traits, however, may impede species recovery following habitat restoration efforts within the species historic range (e.g. dam barrier removal or improved passage) due to their limited rate of dispersal.

Gustatory cues to kinship among males moderate the productivity of females

AbstractMales of many species harm females as a byproduct of intrasexual competition, but this harm can be reduced if males are less competitive in the presence of familiar relatives. We determined the cue males use to identify competitors in this context. We assessed genetic variance in a putative kin recognition trait (cuticular hydrocarbons) in male seed beetles Callosobruchus maculatus and found that five hydrocarbons had significant components of additive genetic variance and could serve as relatedness cues. Next, we tested whether hydrocarbons were the mechanism males use to distinguish the social identities of competitors when strategically adjusting their competitiveness/harmfulness. Pairs of female and male C. maculatus were mated in the presence of hydrocarbons extracted from males that differed in their relatedness and familiarity to the focal male. Females were more productive after mating in the presence of extracts from the focal male’s nonrelatives, if those extracts were also unfamiliar to the focal male. Relatedness had no effect on productivity when extracts were familiar to the focal male. These results may be reconciled with those of previous studies that manipulated the relatedness and familiarity of competing males if the difference between the effect of harmfulness on productivity following a single mating and the effect on lifetime reproductive fitness after multiple matings is accounted for. This study provides a novel demonstration of the mechanism of social recognition in the moderation of sexual conflict.

Transgenerational effects of parental light environment on progeny competitive performance and lifetime fitness.

Plant and animal parents may respond to environmental conditions such as resource stress by altering traits of their offspring via heritable non-genetic effects. While such transgenerational plasticity can result in progeny phenotypes that are functionally pre-adapted to the inducing environment, it is unclear whether such parental effects measurably enhance the adult competitive success and lifetime reproductive output of progeny, and whether they may also adversely affect fitness if offspring encounter contrasting conditions. In glasshouse experiments with inbred genotypes of the annual plant Polygonum persicaria, we tested the effects of parental shade versus sun on (a) competitive performance of progeny in shade, and (b) lifetime reproductive fitness of progeny in three contrasting treatments. Shaded parents produced offspring with increased fitness in shade despite competition, as well as greater competitive impact on plant neighbours. Inherited effects of parental light conditions also significantly altered lifetime fitness: parental shade increased reproductive output for progeny in neighbour and understorey shade, but decreased fitness for progeny in sunny, dry conditions. Along with these substantial adaptive and maladaptive transgenerational effects, results show complex interactions between genotypes, parent environment and progeny conditions that underscore the role of environmental variability and change in shaping future adaptive potential. This article is part of the theme issue 'The role of plasticity in phenotypic adaptation to rapid environmental change'.

Impact of male alternative reproductive tactics on female costs of sexual conflict under variation in operational sex ratio and population density.

Sexual conflict over mating rate is both pervasive and evolutionarily costly. For females, the lifetime reproductive fitness costs that arise through interactions with potential mates will be influenced by the frequency of such interactions, and the fitness cost of each interaction. Both of these factors are likely to be influenced by variation in operational sex ratio (OSR) and population density. Variation in OSR‐ and density‐dependent male alternative reproductive tactics (ARTs) may be particularly important if the fitness costs that females experience vary with the reproductive tactics that males express. Using a simple model, we consider several examples of OSR‐ and/or density‐dependent variation in male ARTs and the frequency of male–female interactions, and find that variation in the expression of male ARTs has the potential to augment or diminish the costs of frequent male interactions for females. Accurately documenting variation in the expression of male ARTs and associated female fitness costs will benefit future work in this area.

A pre‐breeding immune challenge delays reproduction in the female dark‐eyed junco Junco hyemalis

Precise timing of life‐history transitions in predictably changing environments is hypothesized to aid in individual survival and reproductive success, by appropriately matching an animal's physiology and behavior with prevailing environmental conditions. Therefore, it is imperative for individuals to time energetically costly life‐history stages (i.e. reproduction) so they overlap with seasonal peaks in food abundance and quality. Female lifetime reproductive fitness is affected by several factors that influence energy balance, including arrival date, timing of egg production, and energetic condition. Therefore, any extra energetic costs during reproduction may negatively affect timing of egg production, and ultimately a female's fitness. For example, mounting an immunological response elicits a high energetic cost, and this transfer of resources towards cell and immune system maintenance could have direct negative effects on reproductive timing. In order to determine whether an immune challenge delays onset of breeding (i.e. egg production), we administered either a humoral immune challenge (keyhole limpet hemocyanin (KLH)) (treatment) or physiological saline (control) to free‐living female dark‐eyed juncos Junco hyemalis in the period immediately prior to egg‐laying (∼4 weeks). We found that KLH‐injected females artificially delayed clutch initiation when compared to control females. These data help to refine our understanding of how free‐living birds allocate resources between reproduction and self‐maintenance processes during the critical pre‐laying period of the annual cycle.

Recovery and immune priming modulate the evolutionary trajectory of infection-induced reproductive strategies.

In response to parasite exposure, organisms from a variety of taxa undergo a shift in reproductive investment that may trade off with other life-history traits including survival and immunity. By suppressing reproduction in favour of somatic and immunological maintenance, hosts can enhance the probability of survival and recovery from infection. By plastically enhancing reproduction through terminal investment, on the other hand, hosts under the threat of disease-induced mortality could enhance their lifetime reproductive fitness through reproduction rather than survival. However, we know little about the evolution of these strategies, particularly when hosts can recover and even bequeath protection to their offspring. In this study, we develop a stochastic agent-based model that competes somatic maintenance and terminal investment strategies as they trade off differentially with lifespan, parasite resistance, recovery and transgenerational immune priming. Our results suggest that a trade-off between reproduction and recovery can drive directional selection for either terminal investment or somatic maintenance, depending on the cost of reproduction to lifespan. However, some conditions, such as low virulence with a high cost of reproduction to lifespan, can favour diversifying selection for the coexistence of both strategies. The introduction of transgenerational priming into the model favours terminal investment when all strategies are equally likely to produce primed offspring, but favours somatic maintenance if it confers even a slight priming advantage over terminal investment. Our results suggest that both immune priming and recovery may modulate the evolution of reproductive shift diversity and magnitude upon exposure to parasites.

Sex-Specific Allometry of Morphometric and Reproductive Traits in Oriental Fruit Flies (Diptera: Tephritidae).

The oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae), is a highly invasive and polyphagous pest of many horticultural crops in the world, and is currently present in Asia, Africa, and Oceania. To provide essential knowledge for quality control in mass-rearing programs for sterile insect technique against the pest, we investigated how adult body weight and hind-tibial length were correlated in each sex and how body size of each sex affected lifetime reproductive fitness . We show that body weight and hind-tibial length were significantly positively correlated in both sexes, indicating that either trait can be used as an index of body size. However, the weight-tibial length relationships were sex specific, with females gaining disproportionally more weight than males with the increase of hind-tibial length. Body size was not significantly correlated with longevity of either sex, but males lived significantly longer than females. Larger females laid significantly more eggs regardless of body size of the male partner, suggesting that male size has no effect on fecundity. However, body size of both sexes had a significant effect on fertility. We conclude that selection on body size-reproductive fitness relations operates in different directions for the two sexes of B. dorsalis , with larger females and average males having highest reproductive fitness.

The stress of scramble: sex differences in behavior and physiological stress response in a time-constrained mating system

Iteroparous species maximize lifetime reproductive fitness by balancing current and future reproductive investments. In order to maximize fitness in the face of social or environmental heterogeneity, individuals of the same species may vary in whether they prioritize current reproductive opportunity or sacrifice immediate reproduction in order to prioritize survival and future reproductive potential. Glucocorticoid (GC) secretion plays an important role in mediating this trade-off by promoting behavioral and physiological responses associated with survival, often at the expense of nonessential (e.g., reproductive) functions. We used wood frogs (Lithobates sylvaticus [Rana sylvatica]) to test whether males and females differed in their (a) physiological response (plasma corticosterone [CORT] concentration) to standardized handling stress—a proxy for predation threat—and (b) performance of reproductive behaviors that may enhance their conspicuousness to predators. We also tested whether levels of male competition influenced sex differences in these factors, as more intense competition may require males to devote more time to risky reproductive behaviors. We found that females had lower baseline CORT but exhibited a significantly greater CORT response to a stressor and spent less time performing potentially risky behavior (surface floating) than did males. These sex differences were consistent across different levels of male mating competition. Our results reveal that during breeding, males and females may differentially respond to stressors and perform risk-prone behaviors, despite facing the same extreme breeding constraints, providing new insight into the survival-reproduction trade-off of explosively breeding species.

The song of the old mother: Reproductive senescence in female drosophila

Among animals with multiple reproductive episodes, changes in adult condition over time can have profound effects on lifetime reproductive fitness and offspring performance. The changes in condition associated with senescence can be particularly acute for females who support reproductive processes from oogenesis through fertilization. The pomace fly Drosophila melanogaster is a well-established model system for exploring the physiology of reproduction and senescence. In this review, we describe how increasing maternal age in Drosophila affects reproductive fitness and offspring performance as well as the genetic foundation of these effects. Describing the processes underlying female reproductive senescence helps us understand diverse phenomena including population demographics, condition-dependent selection, sexual conflict, and transgenerational effects of maternal condition on offspring fitness. Understanding the genetic basis of reproductive senescence clarifies the nature of life-history trade-offs as well as potential ways to augment and/or limit female fertility in a variety of organisms.

Brotherly love benefits females

Mating competition between males often has harmful consequences for females. But it seems that fruit flies alter their behaviour among kin, with brothers being less aggressive and females reproducing for longer as a result. See Letter p.672 Recent theory suggests that competition between males, a possible cause of harm to females, can be moderated by cooperation between males due to relatedness between them. These authors demonstrate that this is true experimentally by manipulating the relatedness of Drosophila males. Females mated with groups of brothers have greater lifetime reproductive fitness and slower reproductive ageing than those mated with groups of unrelated males. Within the male groups, aggressive behaviour is reduced between brothers, but brothers paired with an unrelated male have reduced reproductive success.

Ejaculate economics: an experimental test in a moth

Increasing evidence shows that spermatogenesis is costly. As a consequence, males should optimize the use of their sperm to maximize their reproductive outputs in their lifetime. However, experimental evidence on this prediction is largely lacking. Here, we examine how a male moth Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) responds to the presence of rivals or additional mates and how such response influences his lifetime reproductive fitness. We show that when rival males are present around a copulating pair, the male ejaculates more sperm to win a sperm competition battle but in such an environment he inseminates fewer females, sires fewer offspring and lives shorter. The opposite is the case when additional females are present during copulation. These findings reveal that elevated reproductive expenditure owing to sperm competition intensity is made at the expense of longevity and future reproduction.

Insect oviposition plasticity in response to host availability: the case of the tephritid fruit fly Bactrocera dorsalis

1. Insect oviposition behaviour is ecologically and physiologically plastic. For tephritid fruit flies, Bactrocera dorsalis Hendel, host availability varies spatially and temporally. Females are expected to adopt adaptive oviposition strategies to maximise lifetime reproductive fitness, including survival. Bactrocera dorsalis oviposition tactics in response to different host availabilities were investigated.2. This study includes three treatments: (i) variable host densities (host density varied according to a fixed cycle from day to day over values of 1, 5, 10 and 20 hosts per cage), (ii) a fixed high host density (20 hosts per cage), and (iii) a fixed low host density (1 host per cage).3. Daily egg‐laying number per female over the course of 27 days was entirely independent of host density and highly dependent on female age. As host availability increased, females accepted significantly more hosts, generally laid small egg clutches, and more broadly distributed the eggs.4. Tephritid fruit flies adaptively adjusted egg clutches in ways that reflected the variability of host availability. Egg‐ and time‐limitation constraints appeared to drive these adjustments. Female egg maturation was triggered by oviposition activity and reflected marked lifetime trade‐offs. Such strategies involved specific time schedules for egg laying.5.This study defined the oviposition plasticity of the tephritid fruit fly. These results have general implications for the behavioural ecology of insect herbivores and parasitoids.

A review of the life cycles and life-history adaptations of pelagic tunicates to environmental conditions

AbstractDeibel, D., and Lowen, B. 2012. A review of the life cycles and life-history adaptations of pelagic tunicates to environmental conditions. – ICES Journal of Marine Science, 69: 358–369. Phylogeny, life cycles, and life-history adaptations of pelagic tunicates to temperature and food concentration are reviewed. Using literature data on lifetime egg production and generation time of appendicularians, salps, and doliolids, rmax, the maximum rate of lifetime reproductive fitness, is calculated as a common metric of adaptation to environmental conditions. The rmax values are high for all three groups, ranging from ∼0.1 to 1.9 d−1, so population doubling times range from ∼8 h to 1 week. These high values of rmax are attributable primarily to short generation times, ranging from 2 to 50 d. Clearly, pelagic tunicates are adapted to event-scale (i.e. days to weeks) rather than seasonal-scale changes in environmental conditions. Although they are not closely related phylogenetically, all three groups have a unique life-history adaptation promoting high lifetime fitness. Appendicularians have late oocyte selection, salps are viviparous, and doliolids possess a polymorphic asexual phase. There has been little research on hermaphroditic appendicularians, on large oceanic salps, and on doliolids generally. Research is needed on factors regulating generation time, on the heritability of life-history traits, and on age- and size-specific rates of mortality.

Seasonal Variation in Sex Ratios Provides Developmental Advantages in White-tailed Deer, <em>Odocoileus virginianus</em>

Since Trivers and Willard first proposed their hypothesis concerning the adaptive advantages of producing a particular offspring sex in relation to maternal condition in 1973, it has been at the forefront of scientific research concerning sex ratios with most subsequent studies focusing on maternal condition as a key contributor to variations in sex ratios. Another factor that could greatly influence sex ratios, although has been only infrequently examined in mammalian species, is birth date. We investigated how birth date influenced offspring sex ratios in White-tailed Deer (Odocoileus virginianus). Since date of birth can greatly influence an individual’s fitness and reproductive success, we suggest that birth date may be an alternative strategy in determining offspring sex ratios. Since it has been shown that the lifetime reproductive fitness of a mother can be increased by producing a particular sex during a particular time, we hypothesized that more male offspring should be born earlier in the season due to their increased reproductive potential from being born at this time. Offspring born earlier will have a head start in development and therefore have greater potential for increased body size and dominance later in life, traits that greatly influence male reproductive success. In this study, we found that maternal condition did not affect offspring sex ratio in a captive population of White-tailed Deer in Michigan; however, birth date did. We found that more males tended to be born during the second and fourth birthing periods, while more females were born during the first, third and fifth periods. In addition, we found that males born earlier in the season had greater mass the following spring than those born later, a trend that was not as dramatic in females. These results lend moderate support to our hypothesis that in White-tailed Deer offspring sex will tend to vary according to timing of birth and relative reproductive advantages gained by a particular sex being born at that time.