Fitness cost of incubation in great tits (Parus major) is related to clutch size

Life-history theory predicts that parents produce the number of offspring that maximizes their fitness. In birds, natural selection on parental decisions regarding clutch size may act during egg laying, incubation or nestling phase. To study the fitness consequences of clutch size during the incubation phase, we manipulated the clutch sizes during this phase only in three breeding seasons and measured the fitness consequences on the short and the long term. Clutch enlargement did not affect the offspring fitness of the manipulated first clutches, but fledging probability of the subsequent clutch in the same season was reduced. Parents incubating enlarged first clutches provided adequate care for the offspring of their first clutches during the nestling phase, but paid the price when caring for the offspring of their second clutch. Parents that incubated enlarged first clutches had lower local survival in the 2 years when the population had a relatively high production of second clutches, but not in the third year when there was a very low production of second clutches. During these 2 years, the costs of incubation were strong enough to change positive selection, as established by brood size manipulations in this study population, into stabilizing selection through the negative effect of incubation on parental fitness.     

Fitness consequences of variable maternal provisioning in quacking frogs (Crinia georgiana)

Variable maternal provisioning may evolve when there is variation in the quality of offspring environments. The frog Crinia georgiana has high variability in egg size both within and between clutches, independent of female phenotype. It breeds in ponds with high spatial and temporal variation in habitat quality. Egg size strongly affected offspring fitness in good and poor quality offspring environments, whether the egg size difference was from between or within clutches. Since there is a trade-off in egg size and number, these fitness consequences translate to strong effects on maternal fitness. In the variable and unpredictable offspring environment of C. georgiana, the maintenance of variable maternal provisioning both within and between clutches is likely to be an evolved response to the offspring environment.     

Experimental demonstration of the insurance value of extra eggs in an obligately siblicidal seabird

A variety of organisms regularly produce more offspring thanthey raise. Despite the apparent energetic waste of such areproductive tactic, overproduction may be favored by naturalselection in some cases. One such case is when surplus offspringcan serve as replacements, or insurance, for failed siblings.We tested the Insurance Egg Hypothesis (IEH) as an explanationfor the overproduction of offspring in an obligately siblicidal seabird, the Nazca booby (Sula grant)i, which fledges a maximumof one nestling regardless of its clutch size. We manipulatedclutch sizes within the range of natural variation encounteredin this species (one-two eggs). The IEH predicts that parentswith two-egg clutches should have higher reproductive successthan those with one-egg clutches because the second egg canprovide a nestling when the first egg fails to hatch, or when the first chick dies young. Consistent with the IEH, naturalone-egg clutches that were enlarged to two eggs produced morehatchlings and fledglings than control one-egg clutches did,and natural two-egg clutches that were reduced to one egg producedfewer hatchlings and fledglings than control two-egg clutchesdid. We also evaluated aspects of the Individual Optimization Hypothesis, which proposes that individual optimal clutch sizesdiffer, as an explanation for clutch size variation in thisspecies. In Nazca boobies, selection driven by replacementvalue appears to favor clutches larger than one even thoughfinal brood size is invariably one. One-egg clutches may be produced by parents experiencing some proximate limitation,such as a lack of food.     

Natural Selection for within-Generation Variance in Offspring Number

In this paper it is shown that natural selection can act on the within-generation variance in offspring number. The fitness of a genotype will increase as its variance in offspring number decreases. The intensity of selection on the variance component is inversely proportional to population size, although the fixation probability of a gene which differs from its allele only in the variance in its offspring number is independent of population size. The concept of effective population size is shown to be of limited use when there is genetic variation in the variance in offspring number.     

Encountering competitors reduces clutch size and increases offspring size in a parasitoid with female-female fighting

Understanding the size of clutches produced by only one parent may require a game-theoretic approach: clutch size may affect offspring fitness in terms of future competitive ability. If larger clutches generate smaller offspring and larger adults are more successful in acquiring and retaining resources, clutch size optima should be reduced when the probability of future competitive encounters is higher. We test this using Goniozus nephantidis, a gregarious parasitoid wasp in which the assumption of size-dependent resource acquisition is met via female-female contests for hosts. As predicted, smaller clutches are produced by mothers experiencing competition, due to fewer eggs being matured and to a reduced proportion of matured eggs being laid. As assumed, smaller clutches generate fewer but larger offspring. We believe this is the first direct evidence for pre-ovipositional and game-theoretic clutch size adjustment in response to an intergenerational fitness effect when clutches are produced by a single individual.     

Selection and constraints on offspring size‐number trade‐offs in sand lizards (Lacerta agilis)

The trade‐off between offspring size and number is a central component of life‐history theory, postulating that larger investment into offspring size inevitably decreases offspring number. This trade‐off is generally discussed in terms of genetic, physiological or morphological constraints; however, as among‐individual differences can mask individual trade‐offs, the underlying mechanisms may be difficult to reveal. In this study, we use multivariate analyses to investigate whether there is a trade‐off between offspring size and number in a population of sand lizards by separating among‐ and within‐individual patterns using a 15‐year data set collected in the wild. We also explore the ecological and evolutionary causes and consequences of this trade‐off by investigating how a female's resource (condition)‐ vs. age‐related size (snout‐vent length) influences her investment into offspring size vs. number (OSN), whether these traits are heritable and under selection and whether the OSN trade‐off has a genetic component. We found a negative correlation between offspring size and number within individual females and physical constraints (size of body cavity) appear to limit the number of eggs that a female can produce. This suggests that the OSN trade‐off occurs due to resource constraints as a female continues to grow throughout life and, thus, produces larger clutches. In contrast to the assumptions of classic OSN theory, we did not detect selection on offspring size; however, there was directional selection for larger clutch sizes. The repeatabilities of both offspring size and number were low and we did not detect any additive genetic variance in either trait. This could be due to strong selection (past or current) on these life‐history traits, or to insufficient statistical power to detect significant additive genetic effects. Overall, the findings of this study are an important illustration of how analyses of within‐individual patterns can reveal trade‐offs and their underlying causes, with potential evolutionary and ecological consequences that are otherwise hidden by among‐individual variation.     

Quantity or quality? Determinants of maternal reproductive success in tropical pythons (Liasis fuscus)

A female''s reproductive output (size and number of offspring) may say little about her reproductive success; the ''quality'' of her progeny and the time that they are produced may be more important in this respect. We marked and released 1224 hatchling water pythons (Liasis fuscus) from 116 clutches of laboratory-incubated eggs, in a study site in tropical Australia. Clutches varied widely in the number of eggs, mean offspring sizes, the proportion of eggs that hatched, and recapture rates of offspring. Clutch size was not significantly correlated with the number of recaptured hatchlings in either year, nor was mean offspring size related to recapture probability. Instead, offspring recapture rates varied as a function of the time of hatching. Recapture rates were higher for hatchlings released in a year with high prey availability than in a year with few prey. In addition, recapture rates were higher for earlier-hatching clutches in the year with few prey. The other significant effect on recapture rates involved offspring viability: some clutches had a much higher proportion of surviving offspring than did others, and recapture rates were higher from clutches with higher hatching success (i.e. proportion of eggs hatching). Hence, the usual measures of reproductive output (clutch size and offspring size) offer only a poor index of a female''s reproductive success in this system.     

Benefits of polyandry: Molecular evidence from field‐caught dung beetles

When females mate with multiple males, they set the stage for postcopulatory sexual selection via sperm competition and/or cryptic female choice. Surprisingly little is known about the rates of multiple mating by females in the wild, despite the importance of this information in understanding the potential for postcopulatory sexual selection to drive the evolution of reproductive behaviour, morphology and physiology. Dung beetles in the genus Onthophagus have become a laboratory model for studying pre‐ and postcopulatory sexual selection, yet we still lack information about the reproductive behaviour of female dung beetles in natural populations. Here, we develop microsatellite markers for Onthophagus taurus and use them to genotype the offspring of wild‐caught females and to estimate natural rates of multiple mating and patterns of sperm utilization. We found that O. taurus females are highly polyandrous: 88% of females produced clutches sired by at least two males, and 5% produced clutches with as many as five sires. Several females (23%) produced clutches with significant paternity skew, indicating the potential for strong postcopulatory sexual selection in natural populations. There were also strong positive correlations between the number of offspring produced and both number of fathers and paternity skew, which suggests that females benefit from mating polyandrously by inciting postcopulatory mechanisms that bias paternity towards males that can sire more viable offspring. This study evaluates the fitness consequences of polyandry for an insect in the wild and provides strong evidence that female dung beetles benefit from multiple mating under natural conditions.     

Aggregative Behavior is Not Explained by an Allee Effect in the Walnut Infesting Fly, Rhagoletis juglandis

Component Allee effects are considered to be a driving force in the origin and maintenance of aggregative behavior. In this study, we examine whether a pattern of active host reuse by the walnut fly, Rhagoletis juglandis Cresson (Diptera: Tephritidae), involves an Allee effect. We examined how the density of clutches deposited within a fruit, the temporal pattern in which successive clutches are deposited and the spatial distribution of clutches over a fruit’s surface influences survival to pupation and pupal size. Within the density range used in this experiment (1 to 7 clutches), increases in larval density strongly reduced pupal weight but not larval survival to pupation. The temporal staggering of clutches into a host strongly reduced offspring survival and, probably owing to competitive release, increased the pupal weight of survivors. Offspring survival and pupal weight were affected relatively little by whether two clutches were deposited within the same oviposition punctures or were evenly spaced. In contrast, in three-clutch treatments offspring survival was higher when clutches were placed within the same oviposition cavity. However, pupal weights did not significantly increase when clutches were placed together and this relatively higher survival rate was not greater than that associated with hosts that contained fewer clutches. The results of the study failed to provide evidence of an Allee effect. We put forward a scenario under which females appear to reuse larval hosts to maximize their own reproductive success, albeit at the expense of the per capita fitness of their offspring.     

Fitness consequences of ovicide in a parasitoid wasp

Ovicide, superparasitism and host rejection are alternative reproductive tactics facing female parasitoid wasps encountering an already-parasitized host. Superparasitism is simply the addition of an egg or a clutch of eggs by the secondary parasitoid, but under ovicide the primary clutch is removed or destroyed. Host rejection occurs if the wasp leaves without laying a clutch. The ectoparasitoid Laelius pedatus (Say) (Hymenoptera: Bethylidae) performs ovicide in this situation. Clutch manipulation experiments show that secondary clutches suffer high mortality in competition with primary clutches, which increases with increasing time delay between clutches. Primary clutches however suffer little in competition with secondary clutches, even if there is minimal time delay between clutches. These data suggest that the offspring of ovicidal females are substantially fitter than the offspring of superparasitizing females. Handling time and clutch size do not differ significantly between first (sole) parasitoids and second (ovicidal) parasitoids. The same is true for offspring survival and development time. However, offspring of second females are slightly smaller. This suggests that parasitized and unparasitized hosts are resources of similar quality when ovicide is performed. These data strongly support the predictions of evolutionary models of ovicide. They may also give some insight into the taxonomic distribution of ovicide in parasitoids.     

INTERACTIVE EFFECTS OF OFFSPRING SIZE AND TIMING OF REPRODUCTION ON OFFSPRING REPRODUCTION: EXPERIMENTAL,MATERNAL, AND QUANTITATIVE GENETIC ASPECTS

We demonstrate that egg size in side-blotched lizards is heritable (parent-offspring regressions) and thus will respond to natural selection. Because our estimate of heritability is derived from free-ranging lizards, it is useful for predicting evolutionary response to selection in wild populations. Moreover, our estimate for the heritability of egg size is not likely to be confounded by nongenetic maternal effects that might arise from egg size per se because we estimate a significant parent-offspring correlation for egg size in the face of dramatic experimental manipulation of yolk volume of the egg. Furthermore, we also demonstrate a significant correlation between egg size of the female parent and clutch size of her offspring. Because this correlation is not related to experimentally induced maternal effects, we suggest that it is indicative of a genetic correlation between egg size and clutch size. We synthesize our results from genetic analyses of the trade-off between egg size and clutch size with previously published experiments that document the mechanistic basis of this trade-off. Experimental manipulation of yolk volume has no effect on offspring reproductive traits such as egg size, clutch size, size at maturity, or oviposition date. However, egg size was related to offspring survival during adult phases of the life history. We partitioned survival of offspring during the adult phase of the life history into (1) survival of offspring from winter emergence to the production of the first clutch (i.e., the vitellogenic phase of the first clutch), and (2) survival of the offspring from the production of the first clutch to the end of the reproductive season. Offspring from the first clutch of the reproductive season in the previous year had higher survival during vitellogenesis of their first clutch if these offspring came from small eggs. We did not observe selection during these prelaying phases of adulthood for offspring from later clutches. However, we did find that later clutch offspring from large eggs had the highest survival over the first season of reproduction. The differences in selection on adult survival arising from maternal effects would reinforce previously documented selection that favors the production of small offspring early in the season and large offspring later in the season—a seasonal shift in maternal provisioning. We also report on a significant parent-offspring correlation in lay date and thus significant heritable variation in lay date. We can rule out the possibility of yolk volume as a confounding maternal effect—experimental manipulation of yolk volume has no effect on lay date of offspring. However, we cannot distinguish between genetic effects (i.e., heritable) and nongenetic maternal effects acting on lay date that arise from the maternal trait lay date per se (or other unidentified maternal traits). Nevertheless, we demonstrate how the timing of female reproduction (e.g., date of oviposition and date of hatching) affect reproductive attributes of offspring. Notably, we find that date of hatching has effects on body size at maturity and fecundity of offspring from later clutches. We did not detect comparable effects of lay date on offspring from the first clutch.     

Eggshell coloration and its importance in postmating sexual selection

Avian eggshell color seems to fulfill multiple functions, some of them being structural and others signaling. In this study, we tested whether or not eggshell coloration may play a role in sexual selection of Tree Sparrows (Passer montanus). According to the “Sexually selected eggshell coloration” hypothesis, eggshell coloration signals female, egg or chick quality and males adjust parental investment according to this signal. Eggs of this species are covered with brown spots and patches, and variation between clutches is high. We found that eggshell coloration correlates with both protoporphyrin and biliverdin, but protoporphyrin concentrations are ten times higher. Eggshell coloration reflects egg and offspring quality, but not female quality. Thus, eggshell coloration may signal female postmating investment in offspring rather than female quality. Furthermore, differential allocation in terms of maternal investment is supported by the fact that females lay more pigmented clutches when mated to males with bigger melanin‐based ornaments relative to their own. Moreover, males invested proportionally more to chicks that hatched from more pigmented clutches. Our correlative results thus seem to support a role of sexual selection in the evolution of eggshell coloration in birds laying brown eggs, pigmented mainly by protoporphyrin.     

No evidence for adjustment of maternal investment under alternative mate availability regimes

Using treatments that mimic high and low availability of reproductive males, it was found that female three‐spined sticklebacks Gasterosteus aculeatus, previously shown to adjust their mate choices when male mates were rare, did not alter their reproductive investment strategies. These results suggest that plasticity in investment is perhaps limited by physiological requirements or dependent on relatively extreme mate availability regimes. The probability of becoming reproductive, number of clutches per season (per female), initial clutch size and mass and the timing of reproduction were all independent of the experience a female had with mate availability. This suggests that pre‐copulatory plasticity in reproductive strategies may contribute more to variation in the strength and direction of sexual selection than reproductive investment in offspring.     

Allocation of offspring size and sex by female black ratsnakes

How females allocate resources to each offspring and how they allocate the sex of their offspring are two powerful potential avenues by which mothers can affect offspring fitness. Previous research has focussed extensively on mean offspring size, with much less attention given to variance in offspring size. Here we focussed on variation in offspring size in black ratsnakes, Elaphe obsoleta . We collected and hatched 105 clutches (1283 eggs) over 9 years. We predicted that females should lay larger eggs, or more variable eggs, when the environment is less predictable. We also predicted that females laying early or laying larger eggs should produce mostly sons because adult males are larger than adult female ratsnakes. The largest hatchling was more than twice the length and almost four times the mass of the smallest hatchling. Variation in offspring size was itself highly variable, with CVs in offspring mass among clutches ranging from 1% to 25%. With one exception, the variables we expected should influence variation in offspring size had little effect. We found that clutch size increased with maternal size and that egg size decreased with clutch size, but we found no evidence that variance in egg size among clutches increased as the season progressed or that females increased the mean size of their offspring the later in the season they laid their eggs. Females in better condition after they finish laying their eggs did produce larger eggs. There was no relationship between within-clutch variation in egg size and laying date or mean egg size. Finally, sex ratio did not vary with mean egg size or hatching date. Given evidence that offspring size in snakes affects survival, selection should reduce variation in offspring size unless that variance enhances maternal fitness and yet we found little support for hypothesized advantages of varying offspring size.     

Variable host quality, life-history invariants, and the reproductive strategy of a parasitoid wasp that produces single sex clutches

The parasitic wasp Achrysocharoides zwoelferi (Hymenoptera, Eulophidae) produces clutches consisting of only one sex. Moreover,male clutch size is invariably one while female clutches arein the range one to four. We designed field experiments todetermine the effect of host quality on clutch composition.We found that solitary male and solitary female clutches werereared from the same size mines, and that larger mines tendedto produce gregarious female clutches. A higher proportionof male clutches were placed in older hosts, despite theirlarge size. Variation in body size, both between and withinclutches, was measured in order to test the predictions of models that take into account the constraint that clutch size is aninteger trait, something of potential importance when absoluteclutch size is low. Our data supported several predictionsof these models, including the trade-off-invariant rule foroptimal offspring size developed by Charnov and Downhower.However, while most invertebrate clutch size models assume equal resource share among members of the same clutch, we found anincrease in inequality in larger clutches.     

Clutch size manipulations in two seed beetles: consequences for progeny fitness

Seed beetles (Coleoptera: Bruchidae) lay their eggs on discrete resource patches, such that competition among larvae for food is an important component of their biology. Most seed beetles, including Stator limbatus, lay eggs singly on individual seeds and avoid superparasitism except when seeds are limiting. In contrast, S. beali, a closely related congener, lays eggs in clutches on a single seed. We tested the hypothesis that natural selection on larval life history characters favors small clutches (selection against large clutches) in S. limbatus, but that selection against large clutches is relaxed in S. beali because of the large size of its host's seeds. We manipulated clutch size and examined its relationship to offspring fitness. Clutch size affected the survivorship of S. limbatus larvae(r ²=0.14), but had no detectable effect on the survivorship of S. beali larvae (r ²=0.04). Also, clutch size had a large effect on development time and body weight of S. limbatus, but not of S. beali. We discuss the implications of this result for the evolution of clutch size in S. limbatus and S. beali.     

Clutch size manipulation, hatching success and offspring phenotype in the ball python (Python regius)

In a diverse array of avian and mammalian species, experimental manipulations of clutch size have tested the hypothesis that natural selection should adjust numbers of neonates produced so as to maximize the number of viable offspring at the end of the period of parental care. Reptiles have not been studied in this respect, probably because they rarely display parental care. However, females of all python species brood their eggs until hatching, but they do not care for their neonates. This feature provides a straightforward way to experimentally increase or reduce clutch size to see whether the mean clutch size observed in nature does indeed maximize hatching success and/or optimize offspring phenotypes. Eggs were removed or added to newly laid clutches of Ball Pythons ( Python regius ) in tropical Africa (nine control clutches, eight with 50% more eggs added, six with 42% of eggs removed). All clutches were brooded by females throughout the 2-month incubation period. Experimental manipulation of clutch-size did not significantly affect the phenotypes (morphology, locomotor ability) of hatchlings, but eggs in 'enlarged' clutches hatched later, and embryos were more likely to die before hatching. This mortality was due to desiccation of the eggs, with females being unable to cover 'enlarged' clutches sufficiently to retard water loss. Our results support the notion of an optimal clutch size, driven by limitations on parental ability to care for the offspring. However, the proximate mechanisms that generate this optimum value differ from those previously described in other kinds of animals. © 2003 The Linnean Society of London . Biological Journal of the Linnean Society 2003, 78 , 263–272.     

Absence of the trade-off between the size and number of offspring in the natterjack toad (Bufo calamita)

Summary A trade-off between size and number of offspring was not found for females of similar sizes of the natterjack toad (Bufo calamita). Moreover, for large females, clutches with higher number of eggs had larger eggs as well. This suggests that larger females produce more numerous and larger eggs because they potentially have more energy available for reproduction. Egg size diminished allometrically with clutch size. Egg size, however, did not increase offspring fitness. Therefore, this allometric decrease may be considered a consequence of phylogenetic constraints rather than a result of optimizing selection.     

Patterns and fitness consequences of intraclutch variation in egg provisioning in tropical Australian frogs

Intraclutch variation in offspring size should evolve when offspring encounter unpredictable environmental conditions. This form of bet-hedging should maximise the lifetime reproductive success of individuals that engage it. We documented the numbers of eggs and means and variances of yolk volume in 15 frog species that occur in tropical savanna woodland. We experimentally determined the effects of initial yolk volume on larval growth patterns in four species. Intraclutch variation in yolk volume occurred to some degree in all species surveyed. Some species had very low, others had very high, intraclutch variation in yolk volume, but all species in which some clutches were highly variable also produced clutches with low variability. Species that occur in areas where the offspring environment is likely to be unpredictable had elevated levels of intraclutch variation in egg provisioning. There was no trade-off between egg size and number in any species surveyed. Under benign laboratory conditions, tadpoles from eggs with larger yolk volumes hatched at larger sizes, and these size differences persisted through a substantial proportion of the larval stage. This indicates that intraclutch variation in egg size has major offspring and thus parental fitness consequences, and is therefore a functional selection variable. This study provides evidence in support of models which predict that intraclutch variation in offspring provisioning can evolve in organisms that reproduce in unpredictable habitats.     

Dispersal duration mediates selection on offspring size

Offspring size varies at all levels of organisation, among species, mothers and clutches. This variation is thought to be the result of a tradeoff between offspring quality and quantity, where larger offspring perform better but are more costly to produce. Local environmental conditions alter the benefits of increased offspring size and thereby mediate selection on this trait. For sessile organisms, dispersal is a crucial part of the offspring phase, and in animals, bigger offspring tend to better endure longer dispersal distances than smaller offspring because they have more energy. Theory predicts that increasing distances between suitable habitats strengthens selection for larger offspring. We manipulated the dispersal duration of offspring of different sizes in the bryozoan Watersipora subtorquata and then examined the relationship between offspring size and post‐metamorphic performance in the field. We found that selection on offspring size is altered by larval experience. Larger offspring had higher post‐settlement performance if the larval period was short but, contrary to current theory, performed worse when the larval period was extended. The reversal of the relationship between offspring size and performance by extending the larval phase in Watersipora may be due to the way in which offspring size affects growth in this species. Regardless of the mechanism, it appears that experiences in one life‐history stage alter selection on offspring size in another stage, even when they occupy identical habitats as adults.