An adaptive annual rhythm in the sex of first pigeon eggs

When the reproductive value of male and female offspring varies differentially, parents are predicted to adjust the sex ratio of their offspring to maximize their fitness (Trivers and Willard, Science 179:90–92, 1973). Two factors have been repeatedly linked to skews in avian offspring sex ratio. First, laying date can affect offspring sex ratio when the sexes differ in age of first reproduction, such that the more slowly maturing sex is overproduced early in the season. Second, position of the egg in the laying sequence of a clutch may affect sex ratio bias since manipulating the sex of the first eggs may be least costly to the mother. We studied both factors in two non-domesticated pigeon species. Both the Wood pigeon (Columba palumbus) and the Rock pigeon (Columba livia) have long breeding seasons and lay two-egg clutches. In the field, we determined the sex of Wood pigeon nestlings. In Rock pigeons, housed in captivity outdoors, we determined embryo sex after 3 days of incubation. On the basis of their sex-specific age of first reproduction, we predicted that males, maturing at older age than females, should be produced in majority early and females later in the year. This was confirmed for both species. The bias was restricted to first eggs. Rock pigeons produced clutches throughout the year and show that the sex of the first egg followed an annual cycle. To our knowledge, this study presents the first evidence of a full annual rhythm in adaptive sex allocation in birds. We suggest that this reflects an endogenous seasonal program in primary sex ratio controlled by a preovulatory mechanism.     

Declining extra-pair paternity with laying order associated with initial incubation behavior,but independent of final clutch size in the blue tit

Although functional explanations for female engagement in extra-pair copulation have been studied extensively in birds, little is known about how extra-pair paternity is linked to other fundamental aspects of avian reproduction. However, recent studies indicate that the occurrence of extra-pair offspring may generally decline with laying order, possibly because stimulation by eggs induces incubation, which may suppress female motivation to acquire extra-pair paternity. Here we tested whether experimental inhibition of incubation during the laying phase, induced by the temporary removal of eggs, resulted in increased extra-pair paternity, in concert with a later cessation of laying, in blue tits (Cyanistes caeruleus). As expected, experimental females showed a more gradual increase in nocturnal incubation duration over the laying phase and produced larger clutches than controls. Moreover, incubation duration on the night after the first egg was laid predicted how extra-pair paternity declined with laying order, with less incubation being associated with more extra-pair offspring among the earliest eggs in the clutch. However, incubation duration on this first night was unrelated to our experimental treatment and independent of final clutch size. Consequently, the observed decline in extra-pair paternity with laying order was unaffected by our manipulation and larger clutches included proportionally fewer extra-pair offspring. We suggest that female physiological state prior to laying, associated with incubation at the onset of laying, determines motivation to acquire extra-pair paternity independent of final clutch size. This decline in proportion of extra-pair offspring with clutch size may be a general pattern within bird species.     

Female house martins (Delichon urbica) reduce egg androgen deposition in response to a challenge of their immune system

Female birds deposit in the yolks of eggs substantial amounts of androgens, such as testosterone and androstenedione. These androgens have been shown to speed up nestling development, induce a fast development of ornaments and increase dominance in adults. Experiments in several species have reported that females invest greater amounts of androgens in the eggs fathered by attractive males, suggesting that yolk androgen is a costly investment for either the offspring or the mother. There is some evidence that nestling immunocompetence may be partially suppressed by high levels of yolk androgens, but it is not known whether this is also the case for females. We tested this hypothesis in the house martin by inducing an immune challenge through an injection of sheep red blood cells, a standard challenge of the humoral immune system. Experimental birds laid eggs with lower amounts of yolk androstenedione than controls, and there was a similar non-significant trend for testosterone. Furthermore, the probability of laying a replacement clutch was higher for birds that had laid a first clutch with relatively high levels of yolk testosterone. These results suggest that yolk androgen deposition is limited by immune costs in the female, and that only females in good condition may afford to invest high levels of androgen in eggs in this species.     

Do female zebrafish withhold reproductive resources for future mating opportunities?

Because polyandry often confers substantial direct and indirect benefits, females might be advantaged if they limit their reproductive investment in a single male when additional partners are available. We tested whether females of the externally fertilizing zebrafish Danio rerio would withhold more of their clutch when immediate further matings were likely. We tested females in three treatments: overnight visual and olfactory exposure to either a single male, two males, or three males. Females were then allowed to mate with one of the males; in the two-male and three-male treatments, the additional males remained in visual and olfactory contact to simulate a high likelihood of additional mating. Available clutch was measured by leaving females to spawn with two novel males for an additional 60?min. In contrast to our expectations, females did not release a greater proportion of their clutch when only a single male was present. Instead, females in the single male treatment released significantly fewer eggs per spawning event and significantly fewer eggs over the full 70?min of the trial. The hypothesis that females adjust current reproductive investment support in relation to the likely availability of mating partners is not supported. Instead, females appear to lay fewer eggs when only one male is available, most likely as a result of physiological stimulation of oocyte maturation, or in response to the likely fertilization capacity of a single individual.     

Differential deposition of antimicrobial proteins in blue tit (Cyanistes caeruleus) clutches by laying order and male attractiveness

Female birds can influence offspring fitness by varying the relative quantities of egg components they deposit within and between clutches. Antimicrobial proteins (lysozyme, ovotransferrin, and avidin) are significant components of the avian albumen and likely aid in defense of embryos from microbial infection. Within clutches, females may enhance antimicrobial defense of early-laid eggs to protect them from the high risk of infection incurred before the onset of incubation. Among entire clutches, females may invest more resources in young sired by more attractive males because they have higher reproductive value. We tested these hypotheses by quantifying antimicrobial protein distribution within and among clutches in blue tit eggs. Contrary to our hypothesis, clutches showed no differential deposition of lysozyme or avidin within clutches, but eggs laid in the middle of the sequence had higher concentrations of ovotransferrin than eggs in the beginning and end. Consistent with our second hypothesis, we found that females produced eggs with higher concentrations of lysozyme (although not ovotransferrin or avidin) when mated to more attractive (more UV-reflective) males. Furthermore, females mated to polygynous males deposited less lysozyme than those mated to monogamous males. These data suggest that allocation of lysozyme at the clutch level may be a maternal effect mediated by male qualities.     

Offspring sex ratios reflect lack of repayment by auxiliary males in a cooperatively breeding passerine

The repayment hypothesis posits that primary sex ratios in cooperative species should be biased towards the helping sex because these offspring “repay” a portion of their cost through helping behavior and therefore are less expensive to produce. However, many cooperatively breeding birds and mammals do not show the predicted bias in the primary sex ratio. Recent theoretical work has suggested that the repayment hypothesis should only hold when females gain a large fitness advantage from the presence of auxiliary adults in the group. When auxiliaries provide little or no fitness advantage, competition between relatives should lead to sex ratios biased towards the dispersing (non-helping) sex. We examined the benefits auxiliaries provide to females and corresponding offspring sex ratios in the red-backed fairy-wren (Malurus melanocephalus), a cooperatively breeding Australian bird with male auxiliary helpers. We found that auxiliaries provide little or no benefit to female reproductive success or survival. As predicted, the population primary sex ratio was biased towards daughters, the dispersing sex, and females with auxiliaries produced female-biased broods whereas females without auxiliaries produced unbiased broods. Moreover, offspring sex ratios were more strongly biased toward females in years when auxiliaries were more common in the population. These results suggest that offspring sex ratios are associated with competition among the non-dispersing sex in this species, and also that females may use cues to assess local breeding opportunities for their offspring.     

Within-clutch egg size asymmetry covaries with embryo sex in the yellow-legged gull Larus michahellis

Non-random sex allocation may occur whenever the expected reproductive value of sons and daughters differs, as is the case when the sexes differ in susceptibility to environmental conditions or maternal effects (e.g. egg size and hatch order). Under such circumstances, covariation between egg and clutch characteristics and egg sex may be expected, and this covariation should vary with maternal state or ecological conditions. In this 2-year study (2007–2008), we examined sex allocation in relation to egg and clutch traits in the yellow-legged gull Larus michahellis, a species where male chicks are larger and more susceptible to harsh rearing conditions than female ones. In 2008, eggs were more likely male early in the season in two- but not three-egg clutches, and large eggs were more likely males late in the season. No egg/clutch traits predicted egg sex in 2007. Within-clutch egg mass asymmetry (the difference in egg mass between the first- and last-laid eggs) predicted sex in both years. In 2007, clutches with smaller egg mass variation were more likely to contain males, while in 2008 this relationship held for the last-laid egg and was reversed for the preceding egg(s). Laying order and sex of the previous egg did not predict egg sex, providing no evidence of sex-specific oocyte clustering. Thus, the relationships between egg sex and egg/clutch traits differed among years, suggesting a phenotypically plastic response of females to extrinsic conditions, and involved within-clutch egg mass asymmetry, a trait likely reflecting variation in maternal quality and/or reproductive tactics, which has been largely neglected in previous studies of sex allocation.     

Sex ratio varies with egg investment in the red-necked phalarope (Phalaropus lobatus)

Fisher’s sex ratio theory predicts that on average parents should allocate resources equally to the production of males and females. However, when the cost/benefit ratio for producing males versus females differs, the theory predicts that parents may bias production, typically through underproduction of the sex with greater variation in fitness. We tested theoretical predictions in the red-necked phalarope, a polyandrous shorebird with sex-role reversal. Since females are larger and therefore potentially more expensive to produce and may have greater variation in reproductive success, we predicted from Fisher’s hypothesis a male bias in population embryonic sex ratio, and from sex allocation theory, female biases in the clutches of females allocating more resources to reproduction. We measured eggs and chicks and sexed 535 offspring from 163 clutches laid over 6 years at two sites in Alaska. The embryonic sex ratio of 51.1 M:48.9 F did not vary from parity. Clutch sex ratio (% male) was positively correlated with clutch mean egg size, opposite to our prediction. Within clutches, however, egg size did not differ by sex. Male phalarope fitness may be more variable than previously thought, and/or differential investment in eggs may affect the within-sex fitness of males more than females. Eggs producing males were less dense than those producing females, possibly indicating they contained more yolk relative to albumen. Albumen contributes to chick structural size, while yolk supports survivorship after hatch. Sex-specific chick growth strategies may affect egg size and allocation patterns by female phalaropes and other birds.     

Dynamics of de novo vitellogenesis in fish with indeterminate fecundity: an application of oocyte packing density theory to European anchovy, <Emphasis Type="Italic">Engraulis encrasicolus</Emphasis>

De novo vitellogenesis is common among teleosts; however, its dynamics and the timing of batch recruitment are poorly understood. In this study, we combine a suite of methods and theories in fish reproductive biology (oocyte packing density, stereology, ovarian allometry, oocyte size frequencies and postovulatory follicle [POF] ageing) to reconstruct the steps and timing of batch recruitment in European anchovy. Using general linear modelling to standardize oocyte numbers, we demonstrate that the fractions of primary growth, cortical alveoli and vitellogenic oocytes in the ovary are relatively stable in females with migratory nucleus oocytes (MN) or with POFs 1 and 2 days old (POF-1 and POF-2), but they change abruptly at hydration. These results imply that batch recruitment in European anchovy occurs in pulses of very short duration (less than a day). The standing crop of vitellogenic oocytes in MN, POF-1 and POF-2 females equals the number of eggs contained in two mature batches.     

Brood sex ratio is dependent on female mating status in polygynous great reed warblers

Females capable of adjusting the sex ratio of their offspring should be more fit than females lacking such an ability. In polygynous birds where breeding success in males is more strongly influenced by body size and/or attractiveness than in females, females might produce more sons when predicting good conditions or when mating with attractive males. Polygynous great reed warbler, Acrocephalusarundinaceus, males direct most of their feeding effort to the primary (first-hatching) nest and in these nests increase their feeding effort in relation to the brood sex ratio (proportion of sons). Therefore, with the expectation of well-nourished sons, we would predict that females which start breeding first within harems might produce more sons than those which start breeding later, and in anticipation of sons with good genes, that females mated to polygynous males might produce more sons than females mated to monogamous males. I took blood samples from hatchlings and determined the sex using DNA markers. The sex ratio of primary (monogamous and polygynous primary) broods is more male-biased (mean 0.58 males, n = 50) than that of secondary (polygynous secondary and tertiary) broods (mean 0.46, n = 25). Moreover, in the secondary broods with the largest clutch (five eggs), in which offspring are most likely to suffer food shortage, the sex ratio was distinctively female biased (mean 0.33, n = 10). In the primary broods, sex ratio was correlated to harem size. The results suggest that great reed warbler females modify the brood sex ratio to produce both well-nourished sons and sons with good genes, but the former effect is probably stronger than the latter factor. Received: 11 March 1998 / Accepted after revision: 23 May 1998     

Intra-specific interactions influence egg composition in the lesser black-backed gull (Larus fuscus)

Egg composition, which is under maternal control, can have a profound effect on offspring fitness. The presence of maternal testosterone and carotenoids in avian egg yolk, for example, is thought to enhance the development and competitive ability of the offspring and protect the hatching and growing chick against oxidative stress. Egg quality often differs between females and such variation can be due to differences in maternal social environment, e.g. breeding density. However, this is confounded by the possibility that the quality of individuals breeding in high- or low-density areas may vary. We tested if maternal social environment influences egg composition in a colonial seabird, the lesser black-backed gull (Larus fuscus). To control for confounding effects of female quality, we experimentally manipulated maternal social environment during egg formation. We increased the frequency of intra-specific interactions (i.e. aggressive encounters with conspecifics other than nest mates) in which the females were involved, by placing an elevated platform in their territory. Females that took part in more intra-specific interactions produced a heavier last egg, but the yolk testosterone concentration in eggs laid by control and experimental females did not differ. Differences in yolk testosterone concentration in relation to embryo sex were found neither in the control nor in the experimental group. In contrast, within the control group, eggs with a male embryo contained more carotenoids than eggs with a female embryo. Moreover, experimental females that had been involved in more intra-specific interactions produced female eggs with higher carotenoid levels compared to female eggs of control birds. An experimental increase in carotenoid levels was not observed in eggs containing a male embryo. Our results suggest that intra-specific interactions experienced by female birds during egg formation can influence conditions for embryonic development.Communicated by J. Graves     

Sexual dimorphism in house sparrow eggs

Recent evidence has revealed an apparently high degree of control by female birds over the physiological aspects of their reproduction and offspring sex allocation, consistent with adaptive hypotheses of sex allocation and differential investment in their offspring. In the house sparrow, we investigated possible mechanisms that may be used by females to enhance the fitness returns from a reproductive effort. Using molecular techniques, we demonstrate that house sparrow eggs containing male embryos are significantly larger than those containing female embryos. We also found that male embryos were laid randomly with respect to laying order. We speculate that this sexual dimorphism of eggs is adaptive, because male house sparrows show greater variance in condition-dependent reproductive success than females. More important, the result provides further evidence of the ability of females to detect or control ovulation of either male or female ova and to differentially invest in one sex over the other. Received: 19 January 2000 / Revised: 29 June 2000 / Accepted 20 July 2000     

Maternal effects on begging behaviour: an experimental demonstration of the effects of laying sequence, hatch order, nestling sex and brood size

Differential resource allocation by females across the laying sequence has been hypothesised as a mechanism through which females could either compensate nestlings that hatch last in asynchronous broods or promote brood reduction. In this study we artificially incubated eggs and cross-fostered offspring to manipulate nestlings’ position in the hatching order, to identify whether the competitive ability of nestlings is dependent on position in the laying sequence. In both control and experimentally reversed broods, first hatched chicks had a higher survival than last hatched siblings. Yet, nestlings that hatched from eggs laid in the second half of a clutch begged with a greater intensity than nestlings hatched from eggs laid in the first half of a clutch. In natural broods, the greater begging competitiveness of nestlings from later-laid eggs led to a moderation of sibling competition and these nestlings achieved the same body size and weight as nestlings from eggs laid in the first half of the clutch. The lack of a substantial difference in the size and condition of surviving nestlings in respect to laying order suggests that differential resource allocation across the egg-laying sequence partially compensates for hatching last in asynchronous broods and reduces the negative effects of the nestling size hierarchy. The effect of laying order, brood size and experimental treatment also differed for male and female nestlings. Our study highlights the need to be aware of the complex and subtle effects of nestling sex and laying sequence when investigating genetic and environmental influences on individual fitness.     

Precise sex allocation, local mate competition, and sex ratio shifts in the parasitoid wasp Trichogramma pretiosum

We determined the sex, order, and clutch size of eggs laid by the parasitoid wasp, Trichogramma pretiosum Riley, in the eggs of one of its natural hosts, Trichoplusia ni (Hübner). The parasitoid allocated sex non-randomly to hosts in the laboratory with a variance significantly less than that of a binomial (random) distribution, our null model. More clutches of two or more eggs contained a single male egg as the second or third egg laid than would be expected by chance and none contained two or more male eggs. T. pretiosum also increased the sex ratio (% male) of its offspring with increasing foundress numbers by increasing the frequency of male offspring as the second egg in a two-egg clutch allocated to unparasitized hosts and as the single egg allocated to previously parasitized hosts. These results indicate that T. pretiosum allocates the sex of its offspring precisely. Precise sex allocation is favored under local mate competition because it reduces variation in the number of sons per patch thus maximizing the number of inseminated daughters emigrating from the patch. Similar combinations of female and male offspring emerged from T. ni eggs parasitized by T. pretiosum in the field, again with a sex ratio variance less than that expected for a binomial distribution. These results strongly suggest that this parasitoid species manifests local mate competition.     

Sex ratio manipulation in response to maternal condition in pigeons: evidence for pre-ovulatory follicle selection

A number of recent reports have documented offspring sex ratio biases in birds. However, to date the potential mechanisms that have been put forward to explain the proximate basis for these deviations are entirely speculative. Using a captive population of domestic pigeons (Columba livia domestica), I tested the hypothesis that mothers in relatively poor physical condition should overproduce daughters by manipulating maternal body condition around the time of egg laying by continuous egg removal and differing feeding regimes. During treatment, females were fed a controlled quantity of food. This, combined with the high energetic costs of repeated egg production caused a significant reduction in maternal body weight. In contrast, during control when food was available ad libitum, maternal body weight did not decline, despite repeated egg production. No significant deviation from parity was evident in the sex ratio of either the first or second eggs during control, whereas during treatment a significant female bias was evident in not only the first egg, but also in the second egg. The absence of single-egg clutches, the rarity of infertile eggs and the lack of laying delays between eggs strongly suggests that the mechanism of sex ratio adjustment in pigeons occurs prior to ovulation. The highly skewed sex-distribution within the two-egg clutches and the unexpectedly large amount of variation in the yolk weight of eggs produced during treatment (but not control) are consistent with the expectations of pre-ovulatory selective resorption of wrong sex ovarian follicles.     

Local mate competition and precise sex ratios in Telenomus fariai (Hymenoptera: Scelionidae), a parasitoid of triatomine eggs

Telenomus fariai is a gregarious endoparasitoid of the eggs of several species of Triatominae (Hemiptera) with a high degree of sibmating: males fertilize their sisters inside the host egg before emergence or emerge first and copulate with their sisters as these emerge. Our results show that, when laying alone, T. fariai behaves adaptively, minimizing offspring mortality and conforming to the prediction of local mate competition (LMC) theory by laying a single male, which is sufficient to fertilize all the sisters. When more than one wasp was placed with one host, sex ratios still conformed to LMC predictions but, despite the decreasing number of eggs laid per wasp, clutch size could not be completely adjusted to avoid mortality. This is not surprising, as superparasitism is rare in the field. Offspring production was independent of the contacts between conspecifics but was affected by the number of mothers laying on a single host egg. The sex of the progeny was precisely determined: a female produced one male per clutch when laying on both unparasitized or previously parasitized hosts. On the other hand, a mother produced less daughters when superparasitizing. Under crowded conditions, the number of eggs laid per female wasp and per host decreased as the number of mothers increased. Developmental mortality also increased with the number of T. fariai eggs per host, determining a maximum of approximately 14 emerged adults. Host resources per individual affected male and female adult size with similar intensity, and male adult mortality was slightly higher than that for females. These results, and previous findings, suggest that T. fariai attains Hamiltonian sex ratios by laying one male and a variable number of females, and that the detection of chemical marks left by conspecifics provides information on the number of foundresses sharing a patch. Received: 4 February 2000 / Received in revised form: 19 April 2000 / Accepted: 20 May 2000     

Helper contributions to reproductive success in the splendid fairy-wren (Malurus splendens)

Summary In Malurus splendens, helpers were present in 65% of 226 group-years with at least one helper female in 37% of group-years. Most females helped for only one year, while many males did so for at least two years. Most were offspring of one or both present breeders, and in 53% of helper-years, helped both parents. For 159 helpers of known age and parentage, the mean coefficient of relatedness to the offspring was 0.47. Novice females with or without helpers produced fewer fledglings per season than females with one year breeding experience and the same level of help. Helpers did not affect production of fledglings per year by females with one year of experience. Females with two or more years experience and at least two helpers produced more fledglings than equivalent birds with one or no helpers. Experience and helpers have little effect on production of fledglings per nest but they lead to more females renesting after a first brood has been raised. Fewer than 20% of novices renest after fledging one brood, while for females with at least two years experience, the percent renesting after success is 40% with no help, 56% with one helper and 69% with 2 or more helpers. Experienced females begin their first clutch earlier than novices, and helpers reduce the time to renest after success from 66 days for an experienced female with no helpers to 50 days for females with at least two years experience and two or more helpers. Breeding females with helpers survive better (76%) than those with no helpers (55%), and helpers thus gain future indirect fitness. Despite their close relatedness to breeders and offspring, in only 19% of group-years did helpers increase their indirect fitness from an increase in productivity.     

Parental condition, brood sex ratio and differential young survival: an experimental study in gulls (Larus fuscus)

Empirical evidence is growing that the offspring sex ratio in birds can be biased in relation to the body condition of parents during breeding. The sex ratio bias may come about because (1) the actual production of the two sexes may be skewed and/or (2) there may be a sex bias in early nestling mortality contingent on parental condition. By manipulating parental condition and giving them a control brood to rear, thereby eliminating effects operating via the eggs, we examined the extent to which parental condition influences the post-hatching survival of male and female lesser black-backed gulls, Larus fuscus. We found that the pre-fledging survival of male chicks was strongly reduced in all-male broods reared by parents in poor condition. Pre-fledging survival of female chicks was, however, unaffected by parental condition or brood sex composition. Thus, independently of any production biases, sex differences in nestling mortality alone can bias the offspring sex ratio at fledging in relation to the prevailing rearing conditions. In other studies on gulls we have, however, also shown that females in poor condition at laying preferentially produce female eggs. Clearly a bias in fledging sex ratio can occur within the same species due to a combination of differential production and differential post-laying mortality; the latter can involve a differential effect of poor egg quality on male and female offspring, differential effects of brood sex composition on their survival and a difference in the capacity of parents to rear males and females. All of these processes need to be taken into account in attempting to understand offspring sex ratios. Received: 15 February 2000 / Revised: 7 August 2000 / Accepted: 26 August 2000     

Yolk androgen deposition as a compensatory strategy

The deposition of androgens into the yolks of eggs can have long-lasting effects on the growth and development of young birds. It has been proposed that female birds and reptiles deposit yolk androgens according to the differential allocation hypothesis (DAH), which posits the allocation of more resources to offspring sired by more attractive, higher-quality males. We examined deposition patterns of yolk androgens in relation to mate attractiveness in the house finch Carpodacus mexicanus. Contrary to the predictions of the DAH, female house finches deposited significantly more androgens into eggs sired by less attractive males. We propose that, rather than serving as resources, androgens are used as mediators in a compensatory distribution strategy, enabling females to improve the quality of young produced with less attractive males.     

Does it matter that male beaugregory damselfish have a mate preference?

Male beaugregory damselfish (Stegastes leucostictus) spent more time courting larger females in both two-choice and single presentations. Female size was significantly correlated with gonad weight. We also verified that female fecundity was extremely variable within a natural population. We found that male reproductive success was highly correlated with both clutch size and clutch number. However, clutch size was not significantly correlated with clutch number, indicating that males that received larger clutches did not receive more egg clutches. Furthermore, there was no difference between the number of offspring produced by males that mated with the largest females and by males that mated with the most females. Thus, although males preferred larger females, males produced similar numbers of offspring by mating with large females or mating with many females. Received: 7 March 1997 / Accepted after revision: 1 November 1997