Reproductive Trade-offs Research Articles

Evaluation of qPCR to Detect Shifts in Population Composition of the Rhizobial Symbiont Mesorhizobium japonicum during Serial in Planta Transfers.

Microbial symbionts range from mutualistic to commensal to antagonistic. While these roles are distinct in their outcome, they are also fluid in a changing environment. Here, we used the Lotus japonicus-Mesorhizobium japonicum symbiosis to investigate short-term and long-term shifts in population abundance using an effective, fast, and low-cost tracking methodology for M. japonicum. We use quantitative polymerase chain reaction (qPCR) to track previously generated signature-tagged M. japonicum mutants targeting the Tn5 transposon insertion and the flanking gene. We used a highly beneficial wild type and moderately beneficial and non-beneficial mutants of M. japonicum sp. nov. to demonstrate the specificity of these primers to estimate the relative abundance of each genotype within individual nodules and after serial transfers to new hosts. For the moderate and non-beneficial genotypes, qPCR allowed us to differentiate genotypes that are phenotypically indistinguishable and investigate host control with suboptimal symbionts. We consistently found the wild type increasing in the proportion of the population, but our data suggest a potential reproductive trade-off between the moderate and non-beneficial genotypes. The multi-generation framework we used, coupled with qPCR, can easily be scaled up to track dozens of M. japonicum mutants simultaneously. Moreover, these mutants can be used to explore M. japonicum genotype abundance in the presence of a complex soil community.

A marriage-market perspective on risk-taking and career choices

We document that women are less likely than men to be in “risky” occupations, i.e., those that exhibit large within-occupation wage dispersion. We first demonstrate that a new theoretical channel—the competitive structure of the marriage market—may incentivize both men and women to choose riskier careers with lower wage returns. We then show that a unifying factor—women’s relative inability to reap the benefits of a risky career due to their shorter reproductive span and consequent career-family trade-off—can help rationalize a set of gender differences in labor-market and marriage-market outcomes. Using data from the United States, we provide empirical evidence that supports the model predictions.

Consumer pressure and supplemental pollination mediate shrub facilitation of a native annual desert plant.

Shrubs are important factors in the assembly of desert plant and animal communities. By providing shelter and resources to other plants and animals, shrubs can change plant-animal interactions including those with consumers and pollinators. Here, we test the hypothesis that shrubs facilitate the reproduction of other desert plants by influencing pollination and compensation for consumer pressure. We used the known benefactor Larrea tridentata as our focal shrub species and the flowering annual Malacothrix glabrata as a potential protege in the Mojave Desert. We tested the effects of facilitation (shrub microsite), consumer pressure (both artificial folivory and florivory), and pollination (ambient or supplemented) on flower and seed production of the annual M. glabrata. We found that floral production and seed mass were similar between microsites but that pollen was limited under shrubs in the absence of any other manipulation. Plants under shrubs produced more flowers and seeds than in the open when folivory and florivory treatments were applied. Malacothrix glabrata experienced a cost to association with L. tridentata in terms of pollen limitation but plants were better able to compensate for consumer pressure under shrubs through increased flower and seed production when damaged. Therefore, association with shrubs involves a reproductive trade-off between costs to pollination and benefits to compensation for consumer pressure.

Desire for social status affects marital and reproductive attitudes: A life history mismatch perspective

Modern low fertility is an unresolved paradox. Despite the tremendous financial growth and stability in modern societies, birth rates are steadily dropping. Almost half of the world's population lives in countries with below-replacement fertility and is projected for a continued decline. Drawing on life history theory and an evolutionary mismatch perspective, we propose that desire for social status (which is increasingly experienced by individuals in industrialized, modern societies) is a key factor affecting critical reproductive preferences. Across two experimental studies (total N = 719), we show that activating a desire for status can lead people to prefer reproductive tradeoffs that favor having fewer children, thereby predicting preferences for delaying both marriage and having a first child. These data support an evolutionary life history mismatch perspective and suggest a complementary explanation for declining fertility rates in contemporary societies, especially developed and economically advanced ones.

Senescence of the immune defences and reproductive trade-offs in females of the mealworm beetle, Tenebrio molitor

In the theory of ageing, it has been assumed that ageing is associated with a decline in somatic defences, including the immune system, as a consequence of a trade-off with reproduction. While overall immunity suffers from age-related deterioration (immune senescence), the different components of the immune response appear to age differently. It is also likely that investment among the many arms of the immune system and reproduction with age is finely adjusted to the organisms' reproductive strategy. We investigated this possibility in females of Tenebrio molitor, a species of long-lived insect with reproductive strategies similar to those of long-lived mammals. We specifically tested the effects of immunological challenges imposed early or late in adult life on immune pathway activation as well as fertility early and late in life. We found complex patterns of changes in immune defences with age and age-specific immune challenges with contrasted relationships with female reproduction. While cellular and enzymatic defences showed signs of ageing, they did not trade-off with reproduction. By contrast, the induced antibacterial immune response was found to be unaffected by age and to be highly connected to female fecundity. These findings suggest that these immunological pathways have different functions with regard to female ageing in this insect species.

Reproductive tradeoffs in a perennial crop: Exploring the mechanisms of coffee alternate bearing in relation to farm management

Like many perennial crops, coffee exhibits alternate bearing, a pattern of reproduction in which high-yielding years are followed by low-yielding ones. Alternate bearing threatens farmer livelihoods, yet little is known about the underlying mechanisms in coffee or the potential for farm management to mitigate it. The resource budget model, an ecological theory positing endogenous resource tradeoffs as the driver of reproductive variability, could help fill this gap. On three coffee farms in Santa María de Dota, Costa Rica, we manipulated relative fruit load, fertilizer levels, and shade cover to test whether the model’s core assumptions (i.e., that fruiting depletes resources and limits investment in subsequent reproduction) can elucidate patterns of alternate bearing in coffee, and to assess whether these patterns are impacted by farm management practices. Coffee plants exhibited within-year and between-year tradeoffs of a high fruit load that scaled from decreased bean size during the same season to fewer fruited nodes and fruits per node in both old and new cohorts of branches during the subsequent season. Stem nitrogen concentration was also depleted in response to high fruit loads and recovered during the subsequent season of low fruiting. The findings provide novel evidence that tradeoffs of a high fruit load are manifested in several reproductive traits at both the branch- and plant-level and offer initial support for the resource budget model in the system. While both moderate shade and increased fertilizer levels tended to improve reproductive traits, a lack of interactive effects between either management treatment and the relative fruit load treatment suggests that they do little to mitigate the reproductive tradeoffs underlying alternate bearing.

Effects of infant age and sex, and maternal parity on the interaction of lactation with infant feeding development in chimpanzees.

The interaction between infant feeding and maternal lactational physiology influences female inter-birth intervals and mediates maternal reproductive trade-offs. We investigated variation in feeding development in 72 immature wild chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda, and made inferences about maternal lactation over the course of infancy. We compared the percentage (%) of time that mothers nursed infants as a function of infant age and assessed how hourly rates and bout durations of nursing and foraging varied in association with differences in offspring age, sex, and maternal parity. Nursing % times, rates and durations were highest for infants ≤ 6 months old but did not change significantly from 6 months to 5 years old. Nursing continued at a decreasing rate for some 5- to 7-year-olds. Infants ≤ 6 months old foraged little. Foraging rates did not change after 1 year old, but foraging durations and the % time devoted to foraging increased with age. Independent foraging probably became a dietary requirement for infants at 1 year old, when their energy needs may have surpassed the available milk energy. Infants spent as much time foraging by the time they were 4 to 5 years old as adults did. No sex effect on infant nursing or foraging was apparent, but infants of primiparous females had higher foraging rates and spent more time foraging than the infants of multiparous females did. Although no data on milk composition were collected, these findings are consistent with a working hypothesis that like other hominoids, chimpanzee mothers maintained a fixed level of lactation effort over several years as infants increasingly supplemented their growing energy, micronutrient and hydration needs via independent foraging. Plateauing lactation may be a more widespread adaptation that allows hominoid infants time to attain the physiology and skills necessary for independent feeding, while also providing them with a steady dietary base on which they could rely consistently through infancy, and enabling mothers to maintain a fixed, predictable level of lactation effort.

Reproductive tradeoffs govern sexually dimorphic tubular lysosome induction in Caenorhabditis elegans.

Sex-specific differences in animal behavior commonly reflect unique reproductive interests. In the nematode Caenorhabditis elegans, hermaphrodites can reproduce without a mate and thus prioritize feeding to satisfy the high energetic costs of reproduction. However, males, which must mate to reproduce, sacrifice feeding to prioritize mate-searching behavior. Here, we demonstrate that these behavioral differences influence sexual dimorphism at the organelle level; young males raised on a rich food source show constitutive induction of gut tubular lysosomes, a non-canonical lysosome morphology that forms in the gut of hermaphrodites when food is limited or as animals age. We found that constitutive induction of gut tubular lysosomes in males results from self-imposed dietary restriction through DAF-7/TGFβ, which promotes exploratory behavior. In contrast, age-dependent induction of gut tubular lysosomes in hermaphrodites is stimulated by self-fertilization activity. Thus, separate reproductive tradeoffs influence tubular lysosome induction in each sex, potentially supporting different requirements for reproductive success.

Detection of reproductive trade-offs is influenced by resource availability and maintenance: an experimental study in the burying beetle (Nicrophorus vespilloides)

Life-history theory predicts trade-offs between investment in current versus future reproduction. However, many studies find no or even positive correlations among these traits. The absence of the trade-off may result from resource availability, as it influences resource allocation to different traits. In addition, since large amounts of resources require additional effort in processing, resource maintenance may affect the detection of reproductive trade-offs. Here, we carried out two breeding attempts to assess the effects of resource availability and maintenance on reproductive trade-offs for both sexes in the burying beetle (Nicrophorus vespilloides). In the first breeding attempt, we simultaneously manipulated carcass size (small versus large) and carcass preparation (non-prepared versus prepared). In the second breeding attempt, we provided parents with same-sized, non-prepared carcasses. For both breeding attempts, we monitored the main and interactive effects of carcass size and carcass preparation on parental effort and reproductive outcome. In the first breeding attempt, males gained more weight and provided more care as carcass size increased, whereas females gained more weight but did not change their care. In addition, when breeding on non-prepared versus prepared carcasses, both parents provided more care and gained more weight. In the second breeding attempt, with increased investment for the first breeding, parents did not show decreased investment for the second brood, vice versa. In contrast, males breeding on large or non-prepared carcasses gained more weight during the first breeding attempt, then provided more care in subsequent reproduction. There were no differences in subsequent female care among different treatments.Significance statementResource availability and resource maintenance may affect the detection of reproductive trade-offs. Here, we simultaneously manipulated carcass size and carcass preparation to assess these effects. This is the first time that the effects of resource availability and resource maintenance on reproductive trade-offs have been separated in burying beetles. Our findings suggest that despite the increased costs of parental care and resource maintenance, parents breeding on large or non-prepared carcasses gained more benefits in terms of increased body weight by staying longer and feeding more from the carcasses. Such benefits gained during the first breeding attempt offset the costs of current reproduction to some degree and masked the reproductive trade-off between current and future reproduction in terms of parental care. These findings enhance the understanding of the effects of resource availability and maintenance on reproductive trade-offs.

An antagonistic pleiotropic gene regulates the reproduction and longevity tradeoff

The antagonistic pleiotropy theory of aging proposes that genes enhancing fitness in early life limit the lifespan, but the molecular evidence remains underexplored. By profiling translatome changes in Caenorhabditis elegans during starvation recovery, we find that an open reading frame (ORF) trl-1 “hidden” within an annotated pseudogene significantly translates upon refeeding. trl-1 mutant animals increase brood sizes but shorten the lifespan and specifically impair germline deficiency–induced longevity. The loss of trl-1 abnormally up-regulates the translation of vitellogenin that produces copious yolk to provision eggs, whereas vitellogenin overexpression is known to reduce the lifespan. We show that the TRL-1 protein undergoes liquid–liquid phase separation (LLPS), through which TRL-1 granules recruit vitellogenin messenger RNA and inhibit its translation. These results indicate that trl-1 functions as an antagonistic pleiotropic gene to regulate the reproduction–longevity tradeoff by optimizing nutrient production for the next generation.

Seasonal trends in adult apparent survival and reproductive trade-offs reveal potential constraints to earlier nesting in a migratory bird.

Birds aim to optimize resources for feeding young and self-maintenance by timing reproduction to coincide with peak food availability. When reproduction is mistimed, birds could incur costs that affect their survival. We studied whether nesting phenology correlated with the apparent survival of American kestrels (Falco sparverius) from two distinct populations and examined trends in clutch-initiation dates. We estimated apparent survival using multi-state mark-recapture models with nesting timing, nesting success, sex, age, and weather covariates. Nesting timing predicted the apparent survival of successful adults; however, the effect differed between populations. Early nesting kestrels had higher apparent survival than later nesters in the western population, where kestrels have a relatively long nesting season. At the eastern site, where kestrels have a relatively short nesting season, the pattern was reversed-later nesters had higher apparent survival than earlier nesters. Nesting timing did not affect the apparent survival of adults with failed nests suggesting that the energetic cost of producing fledglings contributed to the timing effect. Finally, clutch-initiation dates advanced in the western population and remained static in the eastern population. Given that both populations have seasonal declines in productivity, population-specific survival patterns provide insight into seasonal trade-offs. Specifically, nesting timing effects on survival paralleled productivity declines in the western population and inverse patterns of survival and reproduction in the eastern population suggest a condition-dependent trade-off. Concomitant seasonal declines in reproduction and survival may facilitate population-level responses to earlier springs, whereas seasonal trade-offs may constrain phenology shifts and increase vulnerability to mismatch.

The dynamics of disease mediated invasions by hosts with immune reproductive tradeoff

The modern world involves both increasingly frequent introduction of novel invasive animals into new habitat ranges and novel epidemic-causing pathogens into new host populations. Both of these phenomena have been well studied. Less well explored, however, is how the success of species invasions may themselves be affected by the pathogens they bring with them. In this paper, we construct a simple, modified Susceptible-Infected-Recovered model for a vector-borne pathogen affecting two annually reproducing hosts. We consider an invasion scenario in which a susceptible native host species is invaded by a disease-resistant species carrying a vector-borne infection. We assume the presence of abundant, but previously disease-free, competent vectors. We find that the success of invasion is critically sensitive to the infectivity of the pathogen. The more the pathogen is able to spread, the more fit the invasive host is in competition with the more vulnerable native species; the pathogen acts as a ‘wingman pathogen,’ enhancing the probability of invader establishment. While not surprising, we provide a quantitative predictive framework for the long-term outcomes from these important coupled dynamics in a world in which compound invasions of hosts and pathogens are increasingly likely.

Prenatal environmental conditions underlie alternative reproductive tactics that drive the formation of a mixed-kin cooperative society.

Although animal societies often evolve due to limited natal dispersal that results in kin clustering and facilitates cooperation among relatives, many species form cooperative groups with low kin structure. These groups often comprise residents and immigrants of the same sex that compete for breeding opportunities. To understand how these mixed-kin societies form, we investigated the causes and fitness consequences of dispersal decisions in male cooperatively breeding superb starlings (Lamprotornis superbus) inhabiting a climatically unpredictable environment. We show that the two alternative reproductive tactics—natal dispersal or philopatry—exhibit reproductive trade-offs resulting in equivalent lifetime inclusive fitness. Unexpectedly, an individual’s tactic is related to the prenatal environment its parents experience before laying rather than the environment it experiences as a juvenile. Individuals that adopt the tactic not predicted by prenatal environmental conditions have lower fitness. Ultimately, climate-driven oscillating selection appears to stabilize mixed-kin societies despite the potential for social conflict.

Caloric restriction in humans reveals immunometabolic regulators of health span.

The extension of life span driven by 40% caloric restriction (CR) in rodents causes trade-offs in growth, reproduction, and immune defense that make it difficult to identify therapeutically relevant CR-mimetic targets. We report that about 14% CR for 2 years in healthy humans improved thymopoiesis and was correlated with mobilization of intrathymic ectopic lipid. CR-induced transcriptional reprogramming in adipose tissue implicated pathways regulating mitochondrial bioenergetics, anti-inflammatory responses, and longevity. Expression of the gene Pla2g7 encoding platelet activating factor acetyl hydrolase (PLA2G7) is inhibited in humans undergoing CR. Deletion of Pla2g7 in mice showed decreased thymic lipoatrophy, protection against age-related inflammation, lowered NLRP3 inflammasome activation, and improved metabolic health. Therefore, the reduction of PLA2G7 may mediate the immunometabolic effects of CR and could potentially be harnessed to lower inflammation and extend the health span.

Testing the role of testosterone versus estrogens in mediating reproductive transitions in female rhesus macaques

In male vertebrates, testosterone is generally known to coordinate reproductive trade-offs, in part by promoting the transition to the next reproduction at the expense of current parental care. The role of testosterone in reproductive transitions has been little tested in female vertebrates, especially in mammals. The present study sought to fill this gap, by first undertaking an experimental study, in which we identified DHT, androstenediol, and in particular etiocholanolone, as fecal androgen metabolites which reflect serum testosterone concentration in female rhesus macaques (Macaca mulatta). Using concentrations of fecal etiocholanolone as proxy for circulating testosterone, we then conducted a field study on 46 free-ranging rhesus macaques of Cayo Santiago, Puerto Rico, to test if testosterone mediates the trade-off between reproductive transition (a higher chance of reproducing in the next year) and current reproduction (providing more care to current offspring). While the evidence for testosterone was weak, the testing of fecal immunoreactive estrogen metabolites suggested a potential role of estrogen in reproductive trade-offs. We found large individual differences in fecal etiocholanolone concentrations during the early postpartum period that were unexplained even after accounting for sociodemographic factors such as age and dominance rank. Further investigation is needed to understand this variation. Our study suggests that the actions of testosterone in females may not have evolved to fulfil the same role in primate reproductive transitions as it does in males, and we encourage more studies to consider the function of testosterone in reproductive behaviors and life history transitions in females of mammalian taxa.

Varying aerobic capacity in relation to breeding stage and reproductive success in giant petrels (Macronectes spp.)

Reproduction, and parental care in particular, are among the most energy-demanding activities within the annual cycle of adult birds. Parents that cannot meet the metabolic demands and other physiological costs of raising offspring may opt to abandon chicks in favour of self-maintenance and future reproduction. Recent work examining reproductive trade-offs in birds revealed an important role of oxygen carrying capacity in mediating variation in parental effort. This study explores the aerobic factors underlying the success or failure of parental care in two closely-related petrel species during their breeding season on Bird Island, South Georgia: northern giant petrels (Macronectes halli) and southern giant petrels (M. giganteus). Failed breeders of both sexes and species had significantly lower hematocrit levels (by 5.48 ± 0.64%) than successful breeders, and reticulocyte counts also tended to be lower in failed males, consistent with the hypothesis that parental care and workload depend on aerobic capacity. We discuss these results in relation to differences in the foraging ecology of both species and sexes.

Performance Trade-Offs and Resource Availability Drive Variation in Reproductive Isolation between Sympatrically Diverging Crossbills.

AbstractTheoretical models indicate that speciation, especially when the scope for gene flow is great (e.g., sympatric speciation), is most likely when strong performance trade-offs coincide with reproduction. We tested this classic hypothesis using measures of the strength of three prezygotic reproductive isolating barriers (habitat isolation, reduced immigrant fecundity, and behavioral isolation) between two young (~2,000 years) and sympatric red crossbill (Loxia curvirostra) ecotypes. All three isolating barriers increased with increases in performance trade-offs, with total reproductive isolation varying between 0.72 and 1 (0 represents random mating, and 1 represents complete reproductive isolation). Strong trade-offs led to strong habitat isolation, an inability to breed in the "wrong" habitat, and more assortative flocks, with the latter leading to stronger behavioral isolation. Reproductive isolation decreased as resource availability increased relative to the demands of breeding, with higher resource availabilities eliminating the positive relationship between reproductive isolation and performance trade-offs. This latter result is consistent with previous work suggesting that increasing resource abundance dampens the effect of strong performance trade-offs on evolutionary divergence. Because many organisms, with the notable exception of host-specific phytophagous insects, rely on abundant food resources with weak performance trade-offs while breeding, our results may explain why sympatric speciation is uncommon.

Reproductive Tradeoffs in a Perennial Crop: Exploring the Mechanisms of Coffee Alternate Bearing in Relation to Farm Management

Reproductive Tradeoffs in a Perennial Crop: Exploring the Mechanisms of Coffee Alternate Bearing in Relation to Farm Management

Allocation of more reproductive resource to egg size rather than clutch size of gregarious desert locust (Schistocerca gregaria) through increasing oogenesis period and oosorption rate

The desert locust, Schistocerca gregaria, shows a density-dependent reproductive trade-off by laying fewer but larger eggs in crowded conditions (gregarious phase) than in isolated conditions (solitarious phase). However, the physiological mechanisms controlling reproductive resource allocation remain unclear. We examined how egg production processes, including ovulation timing (i.e., oogenesis period), oocyte and ovarian growth rates, and oosorption rate (resorbing developing terminal oocytes), regulate reproductive outputs (egg biomass per clutch, egg size, and clutch size) during a reproductive cycle in S. gregaria by rearing them either under isolated or crowded conditions. We observed a common density-dependent negative correlation between egg size and clutch size, with no significant difference in egg biomass between the two rearing conditions. Dissection of female locusts after different days of oviposition revealed that the daily oocyte growth rate was almost similar between the two rearing conditions, but crowd-reared females ovulated later than isolated-reared ones, resulting in further oocyte growth in the former. Terminal oocytes were renewed by previous penultimate oocytes at the onset of a new reproductive cycle, and oosorption mainly occurred at an early stage in both rearing conditions; however, crowd-reared locusts displayed higher levels of oosorption compared to their isolated-reared counterparts. Crowding induced a high oosorption rate, resulting in a reduced clutch size and a prolonged oogenesis period, which in turn allowed oocytes to intake more yolk, which was probably recycled via oosorption. These results suggest that the length of the oogenesis period and oosorption rate are manipulated by maternal density, and these physiological modifications interactively regulate reproductive trade-off in S. gregaria.

Age-specific mortality and fecundity of a spider mite under diet restriction and delayed mating.

Numerous experimental life-history studies on aging are mainly baised on two classical models-fruit fly Drosophila melanogaster (Meigen) and nematode Caenorhabditis elegans (Maupas)-with relatively little attention given to other organisms with different life-history characters. Two-spotted spider mite Tetranychus urticae Koch (Acari: Tetranychidae) differs from many other arthropods in that the females continue their growth in the early adult stage and can reproduce sexually and asexually. In this study, the influences of dietary restriction and delayed mating on the aging patterns of the spider mite were examined with the prevailing survival and reproduction trade-off hypothesis of aging being tested. Significant sex-specific responses of the spider mites were found. The females showed longevity extension on diet restriction (fasting for 2days in every 4days) compared with their counterparts being fed ad libitum, and after delayed mating for 9days, while the males displayed a decrease in lifespan when experiencing diet restriction but were not significantly influenced by delayed mating. Path analysis was used to investigate the relationship between mite survival and reproduction traits, including longevity, female lifetime reproduction, age at first reproduction, early reproductive efforts and late reproductive efforts, yielding no evidence for trade-offs between these life-history traits. The additive effects of dietary restriction and delayed mating in lifespan extension of female spider mites were confirmed, proving that diet restriction is a robust anti-aging intervention, and that later onset of reproduction can prolong adult lifespan in females.