Lifetime philopatry in the blue-footed booby: a longitudinal study

Philopatry over the lifetime and its relationship with reproductivesuccess were examined using longitudinal records of nest locationand reproduction of individual blue-footed boobies. Males showedshorter natal dispersal than females, and natal dispersal distanceof both sexes were unrelated to either first reproductive successor lifetime reproductive success. Throughout the early lifetime,males and females nested closer to their first breeding sitesthan to their natal sites, and comparison with a simulationof successive breeding dispersals in random directions showedthat male and female blue-footed boobies are philopatric tothe first breeding site. Therefore, throughout the early lifetime,the first breeding site seems to function as a point of referencefor breeding site use together with the previous season's site.Males and females with shorter natal dispersal distances showedstronger lifetime philopatry to their first breeding sites,suggesting stable individual variation in competitive abilityor dispersal phenotype. However, early lifetime philopatry tofirst breeding sites was unrelated to annual breeding success.Compared with simple fidelity to previous breeding sites, lifetimephilopatry to first breeding sites should result in increasedkin interactions and greater selection for kin recognition,altruism and inbreeding avoidance, as well as long-term familiaritywith neighbors.     

Sex-specific sibling interactions and offspring fitness in vertebrates: patterns and implications for maternal sex ratios

Vertebrate sex ratios are notorious for their lack of fit to theoretical models, both with respect to the direction and the magnitude of the sex ratio adjustment. The reasons for this are likely to be linked to simplifying assumptions regarding vertebrate life histories. More specifically, if the sex ratio adjustment itself influences offspring fitness, due to sex-specific interactions among offspring, this could affect optimal sex ratios. A review of the literature suggests that sex-specific sibling interactions in vertebrates result from three major causes: (i) sex asymmetries in competitive ability, for example due to sexual dimorphism, (ii) sex-specific cooperation or helping, and (iii) sex asymmetries in non-competitive interactions, for example steroid leakage between fetuses. Incorporating sex-specific sibling interactions into a sex ratio model shows that they will affect maternal sex ratio strategies and, under some conditions, can repress other selection pressures for sex ratio adjustment. Furthermore, sex-specific interactions could also explain patterns of within-brood sex ratio (e.g. in relation to laying order). Failure to take sex-specific sibling interactions into account could partly explain the lack of sex ratio adjustment in accordance with theoretical expectations in vertebrates, and differences among taxa in sex-specific sibling interactions generate predictions for comparative and experimental studies.     

Context-dependent sex allocation: constraints on the expression and evolution of maternal effects

Despite decades of research, whether vertebrates can and do adaptively adjust the sex ratio of their offspring is still highly debated. However, this may have resulted from the failure of empirical tests to identify large and predictable fitness returns to females from strategic adjustment. Here, we test the effect of diet quality and maternal condition on facultative sex ratio adjustment in the color polymorphic Gouldian finch (Erythrura gouldiae), a species that exhibits extreme maternal allocation in response to severe and predictable (genetically-determined) fitness costs. On high-quality diets, females produced a relatively equal sex ratio, but over-produced sons in poor dietary conditions. Despite the lack of sexual size dimorphism, nutritionally stressed foster sons were healthier, grew faster, and were more likely to survive than daughters. Although these findings are in line with predictions from sex allocation theory, the extent of adjustment is considerably lower than previously reported for this species. Females therefore have strong facultative control over sex allocation, but the extent of adjustment is likely determined by the relative magnitude of fitness gains and the ability to reliably predict sex-specific benefits from environmental (vs. genetic) variables. These findings may help explain the often inconsistent, weak, or inconclusive empirical evidence for adaptive sex ratio adjustment in vertebrates.     

Experimental alteration of litter sex ratios in a mammal

Adaptive theory predicts that mothers would be advantaged by adjusting the sex ratio of their offspring in relation to their offspring's future reproductive success. Studies investigating sex ratio variation in mammals, including humans, have obtained notoriously inconsistent results, except when maternal condition is measured around conception. Several mechanisms for sex ratio adjustment have been proposed. Here, we test the hypothesis that glucose concentrations around conception influence sex ratios. The change in glucose levels resulted in a change in sex ratios, with more daughters being born to females with experimentally lowered glucose, and with the change in glucose levels being more predictive than the glucose levels per se. We provide evidence for a mechanism, which, in tandem with other mechanisms, could explain observed sex ratio variation in mammals.     

Combined influence of maternal and paternal quality on sex allocation in red-capped robins

Sex allocation theory predicts females will adaptively manipulate sex ratios to maximize their progeny's reproductive value. Recently, the generality of biased sex allocation in birds has been questioned by meta-analytic reviews, which demonstrate that many previously reported significant results may simply reflect sampling error. Here, we utilize a robust sample size and powerful statistical approach to determine whether parental quality is correlated with biased sex allocation in red-capped robins. Indices of maternal quality (including interactive effects of age and condition) were strongly related to sex allocation. These relationships were in the predicted directions, with larger effect sizes than those of previous studies in this field. There were also paternal correlates, involving age and the source of paternity. We propose that biased sex allocation occurs in this species, and is maintained by differing production costs of each sex and genetic benefits to females of producing sons when fertilized by high-quality males.     

Dioecy and the evolution of sex ratios in ants

Split sex ratios, when some colonies produce only male and others only female reproductives, is a common feature of social insects, especially ants. The most widely accepted explanation for split sex ratios was proposed by Boomsma and Grafen, and is driven by conflicts of interest among colonies that vary in relatedness. The predictions of the Boomsma–Grafen model have been confirmed in many cases, but contradicted in several others. We adapt a model for the evolution of dioecy in plants to make predictions about the evolution of split sex ratios in social insects. Reproductive specialization results from the instability of the evolutionarily stable strategy (ESS) sex ratio, and is independent of variation in relatedness. We test predictions of the model with data from a long-term study of harvester ants, and show that it correctly predicts the intermediate sex ratios we observe in our study species. The dioecy model provides a comprehensive framework for sex allocation that is based on the pay-offs to the colony via production of males and females, and is independent of the genetic variation among colonies. However, in populations where the conditions for the Boomsma–Grafen model hold, kin selection will still lead to an association between sex ratio and relatedness.     

Reproductive costs of sons and daughters in Rocky Mountain bighorn sheep

Differential maternal investment theory predicts that in sexuallydimorphic and polygynous species mothers should invest morein sons than in daughters. We tested the hypothesis that bighornewes that raise sons incur greater reproductive costs than ewesthat raise daughters. Although ewe mass gain during lactationand subsequent winter body mass loss were independent of lambsex, lambs born the year following the weaning of a son hadlower survival than lambs born after a daughter. The effectsof lamb sex on subsequent reproductive success of ewes becamemore evident at high population density. Lamb sex did not affectmaternal survival. Population density, weather, and ewe agedid not alter the relationship between lamb sex and subsequentreproductive success of the ewe. The year after weaning a son,ewes were more likely to have a daughter than a son, while ewesthat had previously weaned a daughter had similar numbers ofsons and daughters. Our results show that for bighorn sheepewes, sons have a greater life-history cost than daughters,suggesting a differential maternal investment in the sexes.     

Different optimal offspring sizes for sons versus daughters may favor the evolution of temperature-dependent sex determination in viviparous lizards

Temperature-dependent sex determination (TSD) has evolved independently in at least two lineages of viviparous Australian scincid lizards, but its adaptive significance remains unclear. We studied a montane lizard species (Eulamprus heatwolei) with TSD. Our data suggest that mothers can modify the body sizes of their offspring by selecting specific thermal regimes during pregnancy (mothers with higher and more stable temperatures produced smaller offspring), but cannot influence sons versus daughters differentially in this way. A field mark-recapture study shows that optimal offspring size differs between the sexes: larger body size at birth enhanced the survival of sons but reduced the survival of daughters. Thus, a pregnant female can optimize the fitness of either her sons or her daughters (via yolk allocation and thermoregulation), but cannot simultaneously optimize both. One evolutionary solution to reduce this fitness cost is to modify the sex-determining mechanism so that a single litter consists entirely of either sons or daughters; TSD provides such a mechanism. Previous work has implicated a sex difference in optimal offspring size as a selective force for TSD in turtles. Hence, opposing fitness determinants of sons and daughters may have favored evolutionary transitions from genetic sex determination to TSD in both oviparous turtles and viviparous lizards.     

Birth sex ratios relate to mare condition at conception in Kaimanawa horses

Several hypotheses have been proposed to explain variation inbirth sex ratios, based on the premise that variation is expectedwhen the profitability of raising sons and daughters variesbetween individual parents. We tested the Trivers-Willard hypothesisthat mothers in better condition produce relatively more sonsand that mothers in poorer condition produce relatively more daughterswhen male reproductive success is more variable. We examinedbirth sex ratios in relation to mare body condition at conceptionin horses in which male reproductive success is differentiallyhelped by slight advantages in condition. Horses meet the assumptionsof the Trivers-Willard hypothesis better than many species onwhich it has been tested and in which sex ratio biases are notconfounded by sexual size dimorphism such that one sex is more likelyto die in utero in females in poor condition. Mares that hada female foal were in poorer condition at conception than thosethat had a male foal, and mares that had foals of differentsexes in different years were in significantly poorer conditionwhen they conceived their female foal. There was no relationshipbetween offspring sex and mid-gestation condition, and therewas no difference in foaling rates in relation to body conditionat conception. Consequently, sex ratio deviations are not explainedby fetal loss in utero. Furthermore, differential fetal lossof the less viable sex cannot explain the greater proportionof males produced by mares in better condition. Therefore, ourresults suggest that sex ratio modification occurs at conceptionin wild horses.     

Birth sex ratio in captive mammals: Patterns,biases, and the implications for management and conservation

Sex allocation theory predicts that a female should produce the offspring of the sex that most increases her own fitness. For polygynous species, this means that females in superior condition should bias offspring production toward the sex with greater variation in lifetime reproductive success, which is typically males. Captive mammal populations are generally kept in good nutritional condition with low levels of stress, and thus populations of polygynous species might be expected to have birth sex ratios biased toward males. Sex allocation theory also predicts that when competition reduces reproductive success of the mother, she should bias offspring toward whichever sex disperses. These predicted biases would have a large impact on captive breeding programs because unbalanced sex ratios may compromise use of limited space in zoos. We examined 66 species of mammals from three taxonomic orders (primates, ungulates, and carnivores) maintained in North American zoos for evidence of birth sex ratio bias. Contrary to our expectations, we found no evidence of bias toward male births in polygynous populations. We did find evidence that birth sex ratios of primates are male biased and that, within primates, offspring sex was biased toward the naturally dispersing sex. We also found that most species experienced long contiguous periods of at least 7 years with either male‐ or female‐biased sex ratios, owing in part to patterns of dispersal (for primates) and/or to stochastic causes. Population managers must be ready to compensate for significant biases in birth sex ratio based on dispersal and stochasticity. Zoo Biol 19:11–25, 2000. © 2000 Wiley‐Liss, Inc.     

When mothers make sons sexy: maternal effects contribute to the increased sexual attractiveness of extra-pair offspring

Quality differences between offspring sired by the social and by an extra-pair partner are usually assumed to have a genetic basis, reflecting genetic benefits of female extra-pair mate choice. In the zebra finch (Taeniopygia guttata), we identified a colour ornament that is under sexual selection and appears to have a heritable basis. Hence, by engaging in extra-pair copulations with highly ornamented males, females could, in theory, obtain genes for increased offspring attractiveness. Indeed, sons sired by extra-pair partners had larger ornaments, seemingly supporting the genetic benefit hypothesis. Yet, when comparing ornament size of the social and extra-pair partners, there was no difference. Hence, the observed differences most likely had an environmental basis, mediated, for example, via differential maternal investment of resources into the eggs fertilized by extra-pair and social partners. Such maternal effects may (at least partly) be mediated by egg size, which we found to be associated with mean ornament expression in sons. Our results are consistent with the idea that maternal effects can shape sexual selection by altering the genotype-phenotype relationship for ornamentation. They also caution against automatically attributing greater offspring attractiveness or viability to an extra-pair mate's superior genetic quality, as without controlling for differential maternal investment we may significantly overestimate the role of genetic benefits in the evolution of extra-pair mating behaviour.     

Multiple pathways of maternal effects in black-headed gull eggs: constraint and adaptive compensatory adjustment

We investigated in the black-headed gull whether female deposition of antioxidants and immunoglobulins (enhancing early immune function), and testosterone (suppressing immune function and increasing early competitive skills) correlate suggesting that evolution has favoured the mutual adjustment of different pathways for maternal effects. We also took egg mass, the position of the egg in the laying sequence and offspring sex into account, as these affect offspring survival. Yolk antioxidant and immunoglobulin concentrations decreased across the laying order, while yolk testosterone concentrations increased. This may substantially handicap the immune defence of last-hatched chicks. The decrease in antioxidant levels was greater when mothers had a low body mass and when the increase in testosterone concentrations was relatively large. This suggests that female black-headed gulls are constrained in the deposition of antioxidants in last-laid eggs and compensate for this by enhanced testosterone deposition. The latter may be adaptive since it re-allocates the chick's investment from costly immune function to growth and competitive skills, necessary to overcome the consequences of hatching late from an egg of reduced quality.     

Influence of resource level on maternal investment in a leaf-cutter bee (Hymenoptera: Megachilidae)

Fisher's (1930) prediction of equal investment for each sexin a panmictic population is influenced by a number of ecologicalfactors, among which resource availability plays a major role,particularly when the population exists under changing resource availability.Rosenheim et al. proposed a multifaceted parental investment modelbased on the underlying assumption that individual females determine theirsex investment according to resource availability and oocyte availabilityto maximize reproductive success. The model predicts that greater availabilityof resources used for provisions will lead to (1) an increasein the proportion of females produced (when the female is thelarger sex) and (2) an increase in the amount of provisionsper offspring and thus an increase in offspring size. I testedthese predictions by a controlled experiment using a leaf-cutterbee, Megachile apicalis. I presented two levels of food resourcesto the nesting females, which were allowed to forage and nestin cages. The experimental results supported these parentalinvestment model's predictions.     

Parasitism of maternal investment selects for increased clutch size and brood reduction in a host

The allocation of resources to young that will ultimately beleft to die appears counterintuitive. Yet obligate brood reductionhas evolved in a number of species, despite the waste of reproductiveinvestment this may incur. Here we test whether brood parasitismcould be one factor leading to the evolution of obligate broodreduction because surplus eggs in the nest during incubationoffer some protection from the costs of parasitism. Surpluseggs could benefit females in two ways. First, additional eggsmay protect against the direct costs of parasitism by facilitatingrecognition and removal of parasitic eggs with greater accuracy.Second, additional eggs may protect against the indirect costsof parasitism as parasites often damage or remove host eggswhen entering the host nest; surplus eggs may be an essentialinsurance strategy against this damage. We test these possibilitiesin the Montezuma Oropendola (Psarocolius Montezuma), a speciesexperiencing high levels of parasitism by Giant Cowbirds (Scaphiduraoryzivora) throughout their range. Overall rejection rates ofcowbird eggs were high (72%), and experimental addition of parasiticeggs to empty, one-, and two-egg nests demonstrated that recognitionsuccess was unaffected by the presence of additional host eggsfor comparison. However, the value of surplus eggs when oneegg was removed or damaged by a parasite was high; 31.6% ofsuccessful two-egg clutches lost a single egg during incubationand would have failed to produce a chick without a second egg.This was directly attributable to parasitism in at least 33%of all cases. Therefore, despite highly developed host defensesagainst direct costs of parasitism (recognition and removalof parasitic eggs), the associated indirect costs (egg damageand removal) could play an important role in selection for aclutch size that results in more chicks than can be raised.     

Size delays female senescence in a medium sized marsupial: The effects of maternal traits on annual fecundity in the northern brown bandicoot (Isoodon macrourus)

The degree to which females allocate resources between current reproduction, future fecundity and survival is a central theme in life history theory. We investigated two hypotheses proposed to explain patterns of reproductive investment, terminal investment and senescence, by examining the effects of maternal traits (age and maternal mass) on annual fecundity in female northern brown bandicoots, Isoodon macrourus (Marsupialia: Peramelidae). We found that annual fecundity in females declined in their final year of reproduction, indicating reproductive senescence. Maternal mass significantly influenced the rate of senescence and, in turn, a female's lifetime reproductive output. Mass had little effect on fecundity in 1st and 2nd year females, but a positive relationship with fecundity in 3rd year females. This meant that heavy, 3rd year females did not suffer the decline in fecundity shown in light 3rd year females. For 1st year females, mass and leg length increased between their first and second reproductive seasons, indicating a temporary shift, from the allocation of resources to reproduction, to increasing condition or structural size post their first breeding event. There were no net changes to body mass in subsequent years. We suggest that this year of post‐reproductive growth has important consequences for senescent effects on reproduction. Overall, results provided support for the effects of senescence on annual fecundity. Our findings were not consistent with the terminal investment hypothesis; reproductive output did not increase in females' final reproductive season despite a rapid decline in survival. However, this notion cannot be entirely dismissed; other measures of reproductive performance not examined here (e.g. offspring mass) may have provided an indication that females did increase their effort at the end of their lifespan. This study highlights the difficulty of measuring reproductive costs and the importance of understanding the combined effects of specific characteristics of an individual when interpreting reproductive strategies in iteroparous organisms.