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Experimental manipulation of female reproduction reveals an intraspecific egg size-clutch size trade-off.

A negative relationship, or trade-off, between egg size and clutch size is a central and long-standing component of life-history theory, yet there is little empirical evidence for such a trade-off, especially at the intraspecific level. Here, I show that female zebra finches (Taeniopygia guttata) treated chronically during egg formation with the anti-oestrogen tamoxifen lay smaller eggs (by 8%) but produce larger clutches (on average two eggs more) than controls. Decreased egg mass in tamoxifen-treated females was associated with a 50% decrease in plasma levels of the two yolk precursors, vitellogenin and very-low-density lipoprotein. Although tamoxifen-treated females laid more, smaller eggs (and had a higher total expenditure in their clutch), they did not differ from controls in the number of chicks fledged, the mass or size of these chicks at fledging, or the chicks' egg-production performance at three months of age. However, tamoxifen-treated females had lower relative hatching success: they laid more eggs but hatched the same number of chicks. Among individual tamoxifen-treated females, birds that laid the smallest eggs early in their laying sequence laid the largest number of additional eggs, that is, there was a negative correlation, or trade-off, between egg size and clutch size.

Animals↗

Influence of host size on the clutch size and developmental success of the gregarious ectoparasitoid Eulophus pennicornis (Nees) (Hymenoptera: Eulophidae) [corrected] attacking larvae of the tomato moth Lacanobia oleracea (L.) (Lepidoptera: Noctuidae).

The relationship between clutch size, host size and progeny survival in the gregarious ectoparasitoid Eulophus pennicornis was investigated in a number of scenarios. When naive parasitoids were exposed singly to Lacanobia oleracea hosts, clutch size was strongly correlated with the size of the host. However, survival of parasitoid offspring was negatively affected by the size of the host such that, in larger hosts, greater wasp larval and pupal mortality was recorded. As a result, no gain in realised fecundity was achieved through parasitizing L. oleracea larvae of mass >0.4 g over hosts of mass between 0.2-0.3 g. When exposed to populations of mixed stadium hosts (larvae in the fourth, fifth and sixth instars) during the entire lifespan of the wasp, host size and clutch size were correlated in early ovipositions (first three ovipositions). However, as the wasps aged, the relationship was much less apparent. When the parasitoid was restricted to foraging upon populations of sixth instar hosts only, no relationship between host size and clutch size was apparent. Exposure of the parasitoid to mixed and fixed stadium host populations showed that final (sixth) stadium hosts were the most frequently parasitized (ca. 96% of parasitized hosts) and that the average numbers of eggs laid per wasp, and the number of hosts parasitized, was significantly lower when the parasitoid was provided with fourth or fifth instar hosts only. The results indicate that the reproductive success of E. pennicornis does not increase with increasing host size or greater resource availability above a certain threshold, and that the physiological status of the host at the time of parasitism is the governing factor determining oviposition decisions and parasitoid survival. We conclude that E. pennicornis has been selected to preferentially utilize those hosts that maximize progeny survival and to adapt clutch size to the size of such hosts. We hypothesize that the major driver leading to the evolution of this strategy is the ability of the parasitoid to physiologically regulate the host.

Age Factors↗

Body condition, migration, and timing of reproduction in snow geese: a test of the condition-dependent model of optimal clutch size.

The seasonal decline of avian clutch size may result from the conflict between the advantage of early breeding (greater offspring value) and the advantage of a delay in lay date (improved body condition and hence clutch size). We tested predictions of a condition-dependent individual optimization model based on this trade-off (Rowe et al. 1994) in a long-distance migrant, the greater snow goose (Chen caerulescens atlantica), using data on condition, migration, and reproductive decisions of individuals. We closely tracked radio-marked females at their main spring staging area and on their breeding grounds. Our results were consistent with predictions of the model. Early-arriving females had a longer prelaying period and initiated their nests earlier than late arrivals. After controlling statistically for arrival date, we determined that females with high premigration condition had an earlier lay date than those in low condition. After controlling for the seasonal decline (i.e., lay date), we observed that clutch size was not related to premigration condition. Moreover, we took advantage of an unplanned manipulation of the prebreeding condition that occurred during our long-term study. We found that a reduction in condition caused a delay in lay date. However, after controlling for the seasonal decline, it did not affect clutch size. Our study indicates that geese simultaneously adjust their lay date and clutch size according to their premigration condition and migratory behavior as predicted by the condition-dependent optimization model.

Animals↗

Clutch size evolution under sexual conflict enhances the stability of mating systems.

Models of optimal clutch size often implicitly assume a situation with uniparental care. However, the evolutionary conflict between males and females over the division of parental care will have a major influence on the evolution of clutch size. Since clutch size is a female trait, a male has little possibility of directly influencing it. However, the optimal clutch size from a female's perspective will depend on the amount of paternal care her mate is expected to provide. The sexual conflict over parental care will in its turn be affected by clutch size, since a larger clutch makes male care more valuable. Hence, there will be joint evolution of mating system and clutch size. In this paper, we demonstrate that this joint evolution will tend to stabilize the mating system. In a situation with conventional sex roles, this joint evolution might result in either increased clutch size and biparental care or reduced clutch size and uniparental female care. Under some circumstances the initial conditions might determine which will be the outcome. These results demonstrate that it may be difficult to deduce whether biparental care evolved because of few opportunities for breeding males increasing their fitness by attracting additional mates or because of the importance of male care for offspring fitness by studying prevailing mating systems using, for example, male removals or manipulation of males' opportunities for finding additional mates. In general terms, we demonstrate that models of life-history evolution have to consider the social context in which they evolve.

Animals↗

Does clutch size evolve in response to parasites and immunocompetence?

Parasites have been argued to influence clutch size evolution, but past work and theory has largely focused on within-species optimization solutions rather than clearly addressing among-species variation. The effects of parasites on clutch size variation among species can be complex, however, because different parasites can induce age-specific differences in mortality that can cause clutch size to evolve in different directions. We provide a conceptual argument that differences in immunocompetence among species should integrate differences in overall levels of parasite-induced mortality to which a species is exposed. We test this assumption and show that mortality caused by parasites is positively correlated with immunocompetence measured by cell-mediated measures. Under life history theory, clutch size should increase with increased adult mortality and decrease with increased juvenile mortality. Using immunocompetence as a general assay of parasite-induced mortality, we tested these predictions by using data for 25 species. We found that clutch size increased strongly with adult immunocompetence. In contrast, clutch size decreased weakly with increased juvenile immunocompetence. But, immunocompetence of juveniles may be constrained by selection on adults, and, when we controlled for adult immunocompetence, clutch size decreased with juvenile immunocompetence. Thus, immunocompetence seems to reflect evolutionary differences in parasite virulence experienced by species, and differences in age-specific parasite virulence appears to exert opposite selection on clutch size evolution.

Animals↗

The influence of contests on optimal clutch size: a game-theoretic model.

We develop a game-theoretic model to predict the effect of size-dependent contest outcomes on optimal-clutch-size decisions. We consider the case where larger individuals develop from smaller clutches and, as adults, are advantaged in competition for limiting resources. The relationship between fitness and size thus depends on the sizes of other members of the population. We show that clutch-size optima are decreased by body-size-dependent contest outcomes, with larger effects when body size is most affected by clutch size, when prior resource ownership has less influence on contest outcome and when contests occur more frequently. We also show the existence of polymorphisms in clutch-size optima and that clutch-size driven changes in population density can, via an effect on the probability of host finding, further influence optimal clutch size. Our model is formulated to match the life history of a parasitoid wasp, in which clutch size affects offspring size and females engage in direct contests for host ownership, which larger females tend to win; we confirm that female-female competition is likely to influence clutch size in this species. However, the model is also relevant to clutch size in other taxa and supports recent suggestions concerning reproductive decisions in great tits.

Animals↗

Evolution of clutch size in cavity-excavating birds: the nest site limitation hypothesis revisited.

There are two major competing hypotheses for variation in clutch size among cavity-nesting species. The nest site limitation hypothesis postulates that nesting opportunities are more limited for weak excavators, which consequently invest more in each breeding attempt by laying larger clutches. Alternatively, clutch size may be determined by diet; the clutch sizes of strong excavators may be smaller because they are able to specialize on a more seasonally stable prey. We built a conceptual model that integrated hypotheses for interspecific variation in clutch size and tested it with comparative data on life-history traits of woodpeckers (Picidae) and nuthatches (Sittidae). In most analyses, diet explained more variation in clutch size among species than did propensity to excavate. Migratory status was positively associated with clutch size but was difficult to distinguish from diet since resident species consumed more bark beetles (a prey available in winter) and had smaller clutches than migratory species. The literature suggests that cavities are not limited in natural, old-growth forests. Although our data do not rule out nest site limitation, we conclude that annual stability of food resources has a larger impact on the evolution of clutch sizes in excavators than does limitation of nest sites.

Animal Migration↗

[Clutch size, nesting success and breeding success rate in Emberiza jankowskii in the grassland at Baicheng in Jilin Province].

In this article, clutch size, nesting success and breeding success rate of Emberiza jankowskii living in grassland habitats in Baicheng Region of Jilin Province were studied from May to July in 1999. The results showed average clutch size was 5.09 +/- 0.58 eggs per nest. There was negative correlation between clutch size and initial laying date, brood quantity and initial laying date, clutch size and fresh egg weight. There was exceedingly negative correlation between initial laying date and incubated rate. There was exceedingly positive correlation between nest size and clutch size. There was positive correlation between other attributes of nest and clutch size. Average incubation period was 12 +/- 0.94 days, incubated rate was 36.3%, and breeding success rate was 11.11%. The population size of brood size above seven days was 2.56 +/- 1.53. Nestling survival rate was 27.69%.

Animals↗

Female freshwater crayfish adjust egg and clutch size in relation to multiple male traits.

Females may invest more in reproduction if they acquire mates of high phenotypic quality, because offspring sired by preferred partners may be fitter than offspring sired by non-preferred ones. In this study, we tested the differential maternal allocation hypothesis in the freshwater crayfish, Austropotamobius italicus, by means of a pairing experiment aimed at evaluating the effects of specific male traits (body size, chelae size and chelae asymmetry) on female primary reproductive effort. Our results showed that females laid larger but fewer eggs for relatively small-sized, large-clawed males, and smaller but more numerous eggs for relatively large-sized, small-clawed males. Chelae asymmetry had no effects on female reproductive investment. While the ultimate consequences of this pattern of female allocation remain unclear, females were nevertheless able to adjust their primary reproductive effort in relation to mate characteristics in a species where inter-male competition and sexual coercion may mask or obscure their sexual preferences. In addition, our results suggest that female allocation may differentially affect male characters, thus promoting a trade-off between the expression of different male traits.

Animals↗

Evolutionary response to selection on clutch size in a long-term study of the mute swan.

Life-history traits in wild populations are often regarded as being subject to directional selection, and the existence of substantial variation and microevolutionary stasis of these characters is therefore a problem in need of explanation. Avian clutch size is an archetypal life-history trait in this context, and many studies have sought to test explanations for stasis in clutch size. Surprisingly, there are many fewer studies that used long-term data to ask how selection acts on clutch size, particularly in a multivariate framework. In this article, we report selection, inheritance, and evolution of clutch size over 25 years in a colony of mute swans using a multivariate quantitative genetic framework to control for correlations with breeding time. We show that clutch size is influenced by both additive genetic and permanent environmental effects and that selection acts on clutch size in combination with breeding time. Natural selection on clutch size is strongly directional, favoring larger clutches, and we observe an increase in clutch size of 0.35 standard deviations, consistent with the expected response based on selection and inheritance of clutch size. We hypothesize that these changes result from recent relaxation of food constraints and predation risks experienced by this colony.

Animals↗

Parental care and clutch sizes in North and South American birds.

The evolutionary causes of small clutch sizes in tropical and Southern Hemisphere regions are poorly understood. Alexander Skutch proposed 50 years ago that higher nest predation in the south constrains the rate at which parent birds can deliver food to young and thereby constrains clutch size by limiting the number of young that parents can feed. This hypothesis for explaining differences in clutch size and parental behaviors between latitudes has remained untested. Here, a detailed study of bird species in Arizona and Argentina shows that Skutch's hypothesis explains clutch size variation within North and South America. However, neither Skutch's hypothesis nor two major alternatives explain differences between latitudes.

Animals↗

Is clutch size in birds affected by environmental conditions during growth?

Only environmental conditions occurring at the time of breeding have been shown to affect clutch size in birds, even though conditions experienced during growth are known to affect body size or egg size. We show here that environmental conditions experienced during early life can affect clutch size in captive zebra finches (Taeniopygia guttata) and wild great tits (Parus major). Not only do factors outside the immediate breeding season affect clutch size, but clutch size control mechanism is permanently influenced by conditions experienced during ontogeny.

Animals↗

The role of prolactin in the regulation of clutch size and onset of incubation behavior in the American kestrel.

In most bird species, the timing of incubation onset may influence the degree of hatching asynchrony, which, together with variation in clutch size, affects reproductive success. In some domesticated species that usually show no hatching asynchrony, plasma prolactin concentrations in females rise with the onset of incubation and the end of laying, and this rise enhances incubation behavior and may terminate laying. To investigate whether a rise in prolactin during laying is involved in the regulation of clutch size and incubation onset in a species with hatching asynchrony, we measured plasma concentrations of immunoreactive prolactin (ir-prolactin) in laying American kestrels, Falco sparverius, and quantified clutch size and incubation behavior. In a separate study, we administered one of three concentrations of ovine prolactin (o-prolactin) via osmotic pumps implanted in females when egg 2 of a clutch was laid. ir-Prolactin concentrations during laying were higher in small than in large clutches and increased in parallel with the development of incubation behavior. o-Prolactin treatment enhanced incubation behavior, but did not affect clutch size, possibly because the manipulation was performed after clutch size had already been determined. Consistent with studies on domesticated species that show synchronous hatching, our results indicate that rising prolactin during laying enhances the expression of incubation behavior in a species that shows hatching asynchrony. Further studies are necessary to determine whether the relationship between prolactin and clutch size in the American kestrel is one of causation or of mere association.

Animals↗

Do T3 levels in incubating eiders reflect the cost of incubation among clutch sizes?

Complete development of avian eggs requires external heat, inducing in most species an energetic cost of incubation for the parents. Triiodothyronine (T(3)) has been implicated in the control of the metabolic rate and is decreased during fasting in most bird species. This raises the question of the regulation of T(3) during reproduction when incubation (thus heat production) is associated with fasting (and energy sparing). In this study, plasma concentrations of T(3) were studied for different clutch sizes in incubating, as well as in nonincubating, fasting female eiders. Our results show that the T(3) levels decrease during fasting in nonincubating birds, whereas they were maintained during the incubation fast. T(3) levels increased in female eiders at hatching. The plasma T(3) level did not vary among natural clutch sizes in eiders but did so when manipulated. T(3) levels increased when eggs were added (to a maximum of six eggs, i.e., the biggest natural clutch size) or removed (to two eggs, i.e., the smallest natural clutch size). Our results suggest that (1) high T(3) levels during incubation may participate to a threshold of heat production and incubation metabolic rate in eiders despite the fact that they are fasting; (2) since T(3) is associated with the energy expenditure in birds, incubating an enlarged or reduced clutch size may lead to a higher energetic cost of incubation in eiders; and (3) the energy demand of the ducklings at hatching is probably important, as the female T(3) concentrations are then at their highest levels. Thus, any modification of the natural clutch size leads to a rise in the T(3) level of the incubating female, suggesting an additional cost of incubation. Knowing that there is no variation of T(3) levels among natural clutch sizes, this study suggests that a female eider produces a number of eggs corresponding to the energy she can invest in incubation.

Analysis of Variance↗

Natural selection and inheritance of breeding time and clutch size in the collared flycatcher.

Many characteristics of organisms in free-living populations appear to be under directional selection, possess additive genetic variance, and yet show no evolutionary response to selection. Avian breeding time and clutch size are often-cited examples of such characters. We report analyses of inheritance of, and selection on, these traits in a long-term study of a wild population of the collared flycatcher Ficedula albicollis. We used mixed model analysis with REML estimation ("animal models") to make full use of the information in complex multigenerational pedigrees. Heritability of laying date, but not clutch size, was lower than that estimated previously using parent-offspring regressions, although for both traits there was evidence of substantial additive genetic variance (h2 = 0.19 and 0.29, respectively). Laying date and clutch size were negatively genetically correlated (rA = -0.41 +/- 0.09), implying that selection on one of the traits would cause a correlated response in the other, but there was little evidence to suggest that evolution of either trait would be constrained by correlations with other phenotypic characters. Analysis of selection on these traits in females revealed consistent strong directional fecundity selection for earlier breeding at the level of the phenotype (beta = -0.28 +/- 0.03), but little evidence for stabilising selection on breeding time. We found no evidence that clutch size was independently under selection. Analysis of fecundity selection on breeding values for laying date, estimated from an animal model, indicated that selection acts directly on additive genetic variance underlying breeding time (beta = -0.20 +/- 0.04), but not on clutch size (beta = 0.03 +/- 0.05). In contrast, selection on laying date via adult female survival fluctuated in sign between years, and was opposite in sign for selection on phenotypes (negative) and breeding values (positive). Our data thus suggest that any evolutionary response to selection on laying date is partially constrained by underlying life-history trade-offs, and illustrate the difficulties in using purely phenotypic measures and incomplete fitness estimates to assess evolution of life-history trade-offs. We discuss some of the difficulties associated with understanding the evolution of laying date and clutch size in natural populations.

Animals↗

Discrete clutch sizes, local mate competition, and the evolution of precise sex allocation.

Optimal sex allocation under a population structure with local mate competition has been studied mainly in deterministic models that are based on the assumption of continuous clutch sizes; Hamilton's (1967) model is the classic example. When clutch sizes are small, however, this assumption is not appropriate. When taking the discrete nature of eggs into account it becomes critically important whether females control only the mean sex ratio ("binomial" females) or the variance as well ("precise" females). As both types of sex ratio control have been found, it is of interest to investigate their evolutionary stability. In particular, it may be questioned whether perfect control of the sex ratio is always favoured by natural selection when mating groups are small. Models based on discrete clutch sizes are developed to determine evolutionarily stable (ES) sex ratios. It is predicted that when all females are of the binomial type they should produce a lower proportion of daughters than predicted by Hamilton's model, especially when clutch size and foundress number are small. When all females are of the precise type, the ES number of sons should generally be either a stable mixed strategy or a pure strategy, but there are special cases (for two foundresses and particular clutch sizes) where the ES number of sons lies in a trajectory of neutrally stable mixed strategies; the predicted mean sex ratios can be either higher or lower than predicted by Hamilton's model. The existence of ES mixed strategies implies that individual females do not necessarily have to produce sex ratios with perfect precision; some level of imperfection can be tolerated (i.e., will not be selected against). When the population consists of both binomial and precise females, the latter always have a selective advantage. This advantage of precision does not disappear when precision approaches fixation in the population. The latter result contradicts the conclusions of Taylor and Sauer (1980) which is due to their way of expressing selective advantage; they define selective advantage as the between-generation increase per allele, which will always become vanishingly small when an allele reaches fixation, irrespective of fitness differences.

Animals↗

Sex allocation and clutch size in parasitoid wasps that produce single-sex broods.

The parasitoid wasp genus Achrysocharoides (Eulophidae) is unusual in that many of its species lay male and female eggs in single-sex clutches. The average clutch size of female broods is always greater than that of male broods, and in some species male clutch size is always one. We constructed models that predicted that severely egg-limited wasps should produce equal numbers of male and female eggs while severely host-limited wasps should produce equal numbers of male and female broods (and hence an overall female-biased sex ratio). Theory is developed to predict clutch size and sex ratio across the complete spectrum of host and egg limitation. A comparison of 19 surveys of clutch composition in seven species of Achrysocharoides showed a general pattern of equal numbers of male and female broods with a female-biased sex ratio (suggesting host limitation) although with considerable heterogeneity amongst collections and with a number of cases of unexpectedly low frequencies of male broods. Using a previous estimate of the relationship between fitness and size in the field, we predicted the maximally productive (Lack) clutch size for female broods of Achrysocharoides zwoelferi to be three. Of clutches observed in nature, 95% were equal to or smaller in size than the predicted Lack clutch size. When we manipulated local host density in the field, and as predicted by our models, clutch size and the proportion of female broods of A. zwoelferi decreased as hosts became more common, but the absolute frequency of male clutches was lower than expected. Copyright 1998 The Association for the Study of Animal Behaviour.

Journal Article↗