Hatching order and size-dependent mortality in relation to brood sex ratio composition in chinstrap penguins

The differential environmental sensitivity of the sexes hasstrong implications in the evolutionary history of species asit can alter sexual size dimorphism, population sex ratios,and the faculty of parents to manipulate offspring sex in relationto environmental conditions. We studied sexual differences inhatching patterns and evaluated sex- and size-related mortalityin relation to hatching order and brood sex ratios in the chinstrappenguin Pygoscelis antarctica, a moderately size-dimorphic species,with a modal clutch size of 2 eggs. We found that male, second-hatched,and large eggs showed shorter hatching periods than female,first-hatched, and small eggs. We also found a male-biased mortalityof nestlings in the colony. However, male mortality patternsdiffered depending on the brood sex ratio composition. Mortalityof male chicks in all-male broods was higher than in mixed broodsand higher than female mortality in all-female broods. Contrary,females from mixed brood showed higher mortality than theirmale nest mates and higher too than females in all-female broods.Second-hatched chicks also suffered from higher mortality thanfirst-hatched chicks. Our results indicate that both the superiorcompetitive capacity and the higher energy demand of the largersex constitute 2 causal factors explaining patterns of sex-biasedmortality. Both factors occur in the same species and in differentsituations of sibling competition shaped by brood sex ratiocomposition. This study constitutes a good example of how patternsof sex-related mortality can vary depending on nest environmentalcircumstances. Furthermore, our study suggests that hatchingperiod can be a mechanism underlying sexual differences in theembryonic period of birds.     

Sex ratio and fledging success of supplementary-fed Tengmalm's owl broods

A nest box population of Tengmalm's owls (Aegolius funereus) in northern Sweden was studied to investigate the effects of extra food on the sex ratio between hatching and fledging in this sexually size-dimorphic species. The brood size and brood sex ratio of supplementary-fed and control broods were compared. Newly hatched nestlings were blood sampled and sexed by polymerase chain reaction (PCR) amplification of the sex-linked CHD1Z and CHD1W genes. The brood sex ratio at hatching was strongly male biased (65%); this was also the case in broods where all eggs hatched (72%). There was no relationship between hatch order and sex ratio, and hatching sex ratio did not vary significantly with laying date. Brood size decreased between hatching and fledging, but did not differ between fed and control broods at either stage. Brood sex ratio did not differ between hatching and fledging, and fledging sex ratio did not differ between fed and control broods. It was concluded that, at least during the year in which the study was carried out, feeding had no effect on brood reduction, and that male and female nestlings did not show any differential mortality. The mechanisms behind the male-biased sex ratio at hatching, and any possible adaptive reasons for it, are not known.     

No effect of parental quality or extrapair paternity on brood sex ratio in the blue tit (Parus caeruleus)

Sex allocation theory predicts that parents should manipulatebrood sex ratio in order to maximise the combined reproductivevalue of their progeny. Females mating with high quality malesshould, therefore, be expected to produce brood sex ratiosbiased towards sons, as male offspring would receive a relativelygreater advantage from inheritance of their father's characteristicsthan would their female siblings. Furthermore, it has been suggested that sex allocation in chicks fathered through extrapair fertilizations should also be biased towards sons. Contraryto these predictions, we found no evidence that the distributionof sex ratios in a sample of 1483 chicks from 154 broods ofblue tits (Parus caeruleus) deviated significantly from thatof a binomial distribution around an even sex ratio. In addition,we found no significant effect on brood sex ratio of the individualquality of either parent as indicated by their biometrics, feather mite loads, time of breeding, or parental survival. This suggeststhat females in our population were either unable to manipulateoffspring sex allocation or did not do so because selectionpressures were not strong enough to produce a significant shiftaway from random sex allocation. The paternity of 986 chicks from 103 broods was determined using DNA microsatellite typing.Extrapair males sired 115 chicks (11.7%) from 41 broods (39.8%).There was no significant effect of paternity (within-pair versusextrapair) on the sex of individual offspring. We suggest that,in addition to the weakness of selection pressures, the possiblemechanisms responsible for the allocation of sex may not besufficiently accurate to control offspring sex at the levelof the individual egg.     

Sex-biases in the hatching sequence of cooperatively breeding apostlebirds <Emphasis Type="Italic">Struthidea cinerea</Emphasis>

In the cooperatively breeding apostlebird (Struthidea cinerea, Corcoracidae) both sexes are philopatric and help to raise offspring. However, male helpers provision nestlings more often than females, an activity associated with reduced nestling starvation and enhanced fledgling production. Presuming that males are the more helpful sex, we examined the helper repayment hypothesis by testing the predictions that offspring sex ratio should be skewed toward the production of males (a) among breeding groups with relatively few helpers, and (b) in the population as a whole. The relationship between sex and hatching order was examined as a potential mechanism of biasing sex allocation. The sex ratio of all sexed offspring was male biased (57.9%; n = 171) as was the mean brood sex ratio (0.579; n = 70 broods). These biases were less pronounced in the subset of clutches/broods in which all offspring were sexed. This overall bias appeared to result from two distinct patterns of skew in the hatching order. First, mothers in small breeding groups produced significantly more males among the first-hatching pair. This is consistent with the helper repayment hypothesis given that later hatching chicks were less likely to survive, particularly in small groups. Second, almost all fourth-hatching chicks, usually the last in the brood, were male (91.7%, n = 12). This bias is difficult to interpret but demonstrates the value of examining hatching sequences when evaluating specific predictions of sex allocation theory in birds.     

Fledgling sex ratios in relation to brood size in size-dimorphic altricial birds

In six species of dimorphic raptors (females larger than males)and one passerine (males larger than females), the sex ratioat fledging varied systematically with brood size at fledging.In all species the strongest bias toward the smaller sex wasestablished in the largest as well as the smallest broods; amore even distribution of males and females was observed inbroods of intermediate size. We explored a specific differentialmortality explanation for this sex ratio variation. Our hypothesispostulates that variation in mortality is caused by differencesin food demand between broods of the same size, due to theirsex composition. Data from the marsh harrier Circus aeruginosuson gender-related food demand and overall nestling mortalitywere used to predict the frequency of surviving males and femalesat fledging, assuming an even sex ratio at hatching and randommortality with respect to both sexes within broods. The modelquantitatively fits the marsh harrier data well, especiallyin broods originating from large dutches. Although we anticipatethat other mechanisms are also involved, the results supportthe hypothesis of sex-ratio-dependent mortality, differentialbetween broods, as the process generating the observed brood-sizedependence of fledgling sex ratios in sexually dimorphic birds.     

Hatching sex ratio and sex specific chick mortality in common terns Sterna hirundo

Bias in sex ratios at hatching and sex specific post hatching mortality in size dimorphic species has been frequently detected, and is usually skewed towards the production and survival of the smaller sex. Since common terns Sterna hirundo show a limited sexual size dimorphism, with males being only about 1–6% larger than females in a few measurements, we would expect to find small or no differences in production and survival of sons and daughters. To test this prediction, we carried out a 2-year observational study on sex ratio variation in common terns at hatching and on sex specific post hatching mortality. Sons and daughters hatched from eggs of similar volume. Post hatching mortality was heavily influenced by hatching sequence. In addition, we detected a sex specific mortality bias towards sons. Overall, hatching sex ratio and sex specific mortality resulted in fledging sex ratios 8% biased towards females. Thus, other reasons than body size may be influencing the costs of rearing sons. Son mortality was not homogeneous between brood sizes, but greater for two-chick broods. Since adults rearing two-chick broods were younger, lighter and bred consistently later than those rearing three-chick broods, it is suggested that lower capacity of two-chick brood parents adversely affected offspring survival of sons. Though not significantly, two-chick broods tended to be female biased at hatching, perhaps to counteract the greater male-biased nestling mortality. Thus, population bias in secondary sex ratio is not limited to strongly size dimorphic species, but species with a slight sexual size dimorphism can also show sex ratio bias through a combination of differential production and mortality of sons and daughters.     

Experimental manipulation of maternal effort produces differential effects in sons and daughters: implications for adaptive sex ratios in the blue-footed booby

Sex allocation theory predicts that mothers in good conditionshould bias their brood sex ratio in response to the differentialbenefits obtained from increased maternal expenditure in sonsand daughters. Although there is well-documented variationof offspring sex ratios in several bird species according tomaternal condition, the assumption that maternal condition has different fitness consequences for male and for female offspringremains unclear. The blue-footed booby (Sula nebouxii) is asexually size-dimorphic seabird, with females approximately31% heavier than males. It has been reported that the sex ratiois male biased in years with poor feeding conditions, whichsuggests that either females adjust their sex ratio in accordancewith their condition or that they suffer differential brood mortality before their sex can be determined. In this studyI tested whether the condition of mothers affected their daughters'fitness more than their sons' fitness. I manipulated maternalinvestment by trimming the flight feathers and thereby handicappingfemales during the chick-rearing period. Adult females in thehandicapped group had a poorer physical condition at end ofchick growth, as measured by mass and by the residuals of masson wing length compared to control birds. Female chicks wereaffected by the handicapping experiment, showing a lower massand shorter wing length (reduced approximately 8% in both measures)than controls. However, this effect was not found in male chicks.Hatching sex ratios were also related to female body conditionat hatching. The brood sex ratio of females in poor conditionwas male biased but was female biased for females in good condition.Overall, these results suggest that the variation in the sexratio in blue-footed boobies is an adaptive response to thedisadvantage daughters face from being reared under poor conditions.     

Sex ratio and male sexual characters in a population of blue tits, Parus caeruleus

Sex allocation theory proposes that parents should bias thesex ratio of their offspring if the reproductive value of onesex is greater than that of the other. In the monogamous bluetit (Parus caeruleus), males have a greater variance in reproductivesuccess than females, and high-quality males have higher reproductivesuccess than high-quality females due to extrapair paternity.Consequently, females mating with attractive males are expectedto produce broods biased toward sons, as sons benefit more thandaughters from inheriting their father's characteristics. Songand plumage color in birds are secondary sexual characters indicatingmale quality and involved in female choice. We used these malesexual traits in blue tits to investigate adaptive sex ratiomanipulation by females. We did not find any relationship betweenmale color ornamentation and brood sex ratio, contrary to previousstudies. On the other hand, the length of the strophe bout (i.e.,the mean number of strophes per strophe bout) of fathers waspositively related with the proportion of sons in their broods.The length of the strophe bout is supposed to reflect male qualityin terms of neuromuscular performance. We further showed thatsons produced in experimentally enlarged broods had shorterstrophe bouts than sons raised in reduced broods. These resultsare consistent with the hypothesis that females adjust the sexratio of their broods in response to the phenotype of theirmate.     

Brood desertion in Kentish plover: sex differences in remating opportunities

To understand the evolution of parental care, one needs to estimatethe payoffs from providing care for the offspring and the payoffsfrom terminating care and deserting them. These payoffs arerarely known. In this study we experimentally estimated therewards from brood desertion in a species that has a variablepattern of parental care. In particular, either the female or themale parent may desert the brood in Kentish plover Charadrius alexandrinus,so some broods are attended by one parent of either sex, whereasin other broods both parents stay with the brood until the chicks fledge.We created single males and single females by experimentallyremoving the other parent and the clutch. The expected rematingtime of males was significantly higher (median: 25.4 days) thanthat of the females (5.3 days, p <.0001). The expected rematingtime tended to increase over the breeding season in both sexes,although the increase was significant only in females. The newnest of remated males was closer to their previous territory (mean± SE, 46 ± 8 m) than that of the remated females(289 ± 57 m, p <.001). Hatching success of new nestswas not different between remated males and females. Our resultsdemonstrate that the remating opportunities are different formale and female Kentish plovers and these opportunities varyover the season. We propose that the remating opportunitieswere influenced by the male-biased adult sex ratio and the seasonaldecrease in the number of breeders. However, we stress thatmeasuring remating times is a more direct measure of matingopportunities than calculating the operational sex ratio.     

Unusual pattern of sex‐specific mortality in relation to initial brood sex composition in the black‐billed magpie Pica pica

In sexually size‐dimorphic species, brood sex composition may exert differential effects on sex‐specific mortality. We investigated the sex‐specific mortality and body condition in relation to brood sex composition in nestlings of the black‐billed magpie Pica pica. Neither significantly sex‐biased production at hatching nor overall sex‐biased mortality during the nestling period was found. Sex‐specific mortality as a function of brood sex composition, however, differed between female and male nestlings. We found higher mortality for females in male‐biased broods and higher mortality for males in female‐biased broods, a phenomenon that we call ‘rarer‐sex disadvantage’. As a result, fledging sex ratios became more biased in the direction of bias at hatching, a phenomenon that cannot be readily explained by previous hypotheses for sex‐specific mortality. Two temporal variables, fledging date and laying date, were also correlated with sex‐specific mortality: female nestlings in earlier broods experienced higher mortality than male nestlings whereas male nestlings in later broods experienced higher mortality. We suggest that this unusual pattern of mortality may be explained by adaptive adjustments of brood sex composition by parents, either through the effects of a slight sex difference in offspring dispersal patterns on parental fitness, or owing to sex differences as regards the benefits of early fledging.     

Spiderling sex ratio and maternal investment in the bolas spider Mastophora cornigera (Araneae,Araneidae)

Male Mastophora cornigera exit egg sacs as adults, which allowed us to determine spiderling sex ratios and patterns of maternal investment in this species. We collected 15 egg sacs produced by seven mothers, which yielded 1945 emergent spiderlings which were sexed, 1850 of which were weighed. Two emergent broods were significantly male and female biased and were unaffected by pre-emergence mortality. The weights of male and female spiderlings differed in eight broods, with males and females being heavier in four cases each. Five of these broods were derived from multiple egg sac sets produced by one mother, and in each case, the total mean male and female spiderling weights for all broods in a set were biased in the same direction as the biased brood(s) within that set. Mean emergent spiderling weight was independent of brood size and sex ratio for both males and females. Despite such independence, sex allocation in M. cornigera can favor sons, daughters, or both equally, and by numbers, by weight, or both at once. The proximate mechanisms and adaptive significance of such variability is unknown. We also review evidence for gender-biased allocations in arachnid offspring and suggested mechanisms for their applicability to M. cornigera.     

Insemination Capacity and Dispersal in Relation to Sex Allocation Decisions in Goniozus legneri (Hymenoptera: Bethylidae): Why Are There More Males in Larger Broods?

Models considering sex ratio optima under single foundress strict local mate competition predict that female bias will be reduced by stochasticity in sex allocation, developmental mortality of males and limited insemination capacity of males. In all three cases the number of males per brood is expected to increase with brood size. Sex ratio optima may also be less female biased when several mothers contribute offspring to local mating groups or if non‐local mating occurs between members of different broods; again more males are expected in larger broods. In the parasitoid wasp Goniozus legneri (Hymenoptera: Bethylidae), sex allocation has only a small stochastic component, developmental mortality is low and non‐siblings are unlikely to develop in the same brood. However, the number of males per brood increases with the size of the brood (produced by a single mother). We investigated the further possibilities of limited insemination capacity and non‐local mating using a naturalistic experimental protocol. We found that limited insemination capacity is an unlikely general explanation for the increase in number of males with brood size. All males and females dispersed from both mixed and single sex broods. Although most females in mixed sex broods mated prior to dispersal, these data suggest that non‐local mating is possible, for instance via male immigration to broods containing virgin females. This may influence sex ratio optima and account for the trend in male number.     

Sex-specific hatching order, growth rates and fledging success in jackdaws Corvus monedula

In the jackdaw Corvus monedula , eggs hatch asynchronously with the youngest chicks in the brood often starving to death. So far, it is unknown whether there are sex differences in vulnerability to starvation. Adult females are smaller than males suggesting that daughters should be cheaper to produce than sons and so, less likely to starve when nest conditions are poor. Here, we determine whether sex, laying order and season interact to influence growth and fledging success. In a nestbox population of jackdaws, we found a non-significant female bias at both hatching (112:120) and fledging (37:52). Generalised linear models revealed that parents seemed to be investing differently in sons and daughters depending on their chances of success. Broods produced late in the season were significantly female biased, particularly those from small clutches. Females hatched towards the end of the season, when conditions were poor, were more likely to fledge than males. Nestlings that were relatively large at hatching were more likely to fledge. This effect was particularly important for last hatched individuals. Overall, males had a higher mortality rate than females. The most likely cause was starvation due to higher energetic requirements, because males were larger than females at fledging. We suggest that in species with brood reduction, sex-biased mortality may be at least as important as primary sex ratio manipulation in determining avian sex ratios.     

Female body condition and brood sex ratio in Yellow-legged Gulls Larus cachinnans

In the Yellow-legged Gull Larus cachinnans , males are the larger sex, and show more reproductive variance than females. We predicted that the proportion of male chicks in a brood should increase with female body condition. We investigated brood sex ratio by using DNA markers taken from samples of hatchlings or dead embryos, and female body condition using plasma cholesterol concentration as a reliable indicator. The brood sex ratio of females in good condition was male biased and the sex ratio of females in poor condition was female biased. This relationship was also significant in those nests where all the eggs laid were sexed. Thus, manipulation of embryo mortality cannot explain the biases reported in this study, suggesting that the sex ratio of the eggs was biased prior to laying. These results confirm that sex-ratio manipulation in gulls operates under natural conditions, and supports earlier experimental findings.     

Sex ratios and sexual selection in socially monogamous zebra finches

An experiment was performed in which adult sex ratios of zebrafinches, Taeniopygyia guttata castanotis, were varied to testpossible effects of adult population sex ratios on sexual selectionintensity and mating system dynamics in species with biparentalcare. The possibility that sex ratio influences the successof social mating patterns (leading to polygyny when males arerare and polyandry when females are rare) was not supported.Results did support the prediction of the differential allocationhypothesis that individuals of the abundant sex would increasetheir relative parental expenditure (PE). Although total (male+ female) PE did not vary between treatments, relative malePE was significantly higher in the male-biased treatment (MBT;sex ratio 64% male) than in the female-biased treatment (FBT; sexratio 36% male). In both treatments, male PE contributions contributedto female reproductive rate. Results also supported the predictionof the differential access hypothesis that individuals of theabundant sex would experience greater intensity of selectionon sexually selected attributes. Male beak color, a sexuallyselected trait, influenced male social parentage in the MBTbut not in the FBT. Finally, broods in the FBT displayed higher hatchingasynchrony and lower hatching success; we believe this was causedby early onset of incubation, a tactic used as a defense againstintraspecific brood parasitism, which was much higher in theFBT. Population sex ratios may be an important factor affectingfemale ability to influence male parental investment patterns.     

Evidence for Strategic Sex Allocation in the Guppy (Poecilia reticulata): Brood Sex Ratio and Size Predict Subsequent Adult Male Mating Success

Sex allocation theory predicts that females should produce more sons when the reproductive success of sons is expected to be high, whereas they should produce more daughters, not daughters when the reproductive success of sons is expected to be low. The guppy (Poecilia reticulata) is a live‐bearing fish, and female guppies are known to produce broods with biased sex ratios. In this study, we examined the relationship between brood sex ratio and reproductive success of sons and daughters, to determine whether female guppies benefit from producing broods with biased sex ratios. We found that sons in male‐biased broods had greater mating success at maturity than sons in female‐biased broods when brood sizes were larger. On the other hand, the reproductive output of daughters was not significantly affected by brood sizes and sex ratios. Our results suggest that female guppies benefit from producing large, male‐biased brood when the reproductive success of sons is expected to be high.     

Seasonal shifts in sex ratios of fledgling American kestrels (Falco sparverius paulus): The Early Bird Hypothesis

We document a seasonal shift in the sex ratios of broods produced by resident southeastern American kestrels (Falco sparverius paulus) breeding in nest boxes in Florida. Early in the breeding season, most biased broods were biased towards males, whereas later in the season, most biased broods were biased towards females. Computer-simulated broods subjected to sex-biased egg and/or nestling mortality demonstrate that it is possible that differential mortality produced the pattern of bias that we observed. However, these simulations do not exclude the possibility that female kestrels were manipulating the primary sex ratio of the broods. We present evidence that this sex ratio shift is adaptive: for males we detected breeding as yearlings, all had fledged early the previous season. No such relationship between season and the probability of breeding as a yearling was found for females. We propose the Early Bird Hypothesis as the ecological basis for the advantage of fledg ing early in males. We hypothesize that pre-emptive competition among post-fledging, dispersing males for breeding sites confers an advantage to males fledged early in the season. This hypothesis may explain why a non-migratory population of the Eurasian kestrel (F. tinnunculus) and non-migratory American kestrels breeding in Florida (F. s. paulus) exhibit this seasonal shift in sex ratios, whereas migratory American kestrels (F. s. sparverius) breeding in Saskatchewan, Canada, do not. We discuss the relevance of the Early Bird Hypothesis for other animal species.     

Brood desertion in Kentish Plover Charadrius alexandrinus: an experimental test of parental quality and remating opportunities

Uniparental male care combined with polyandry is rare in birds, and the best known examples are in shorebirds Charadrii. There are two current hypotheses explaining why males care for the brood, whereas females desert and remate: either males are more capable than females at providing uniparental care (“parental quality hypothesis”) or females gain a greater increase in reproductive success by deserting than do males (“remating opportunity hypothesis”). I experimentally tested both hypotheses in Kentish Plover Charadrius alexandrinus, one of the few avian species in which either parent may desert the brood. By experimentally removing one parent when the chicks hatched, I found that male-tended broods had better survival than female-tended ones, particularly up to 6 days after hatching. It is unlikely that differential brood mortality was caused by chilling of the chicks, since the brooding behaviour of males and females was not different. The results of this study are consistent with the explanation that male-tended broods survived better because males were better able to protect the brood from attacks by conspecifics and predators. The remating opportunity hypothesis was also corroborated because single females acquired new mates faster than did single males. The results of this study suggest that both the better parental capability of males and the greater remating opportunities of females predispose Kentish Plovers for uniparental male care, desertion by the female parent and sequential polyandry.     

Complex sex allocation in the laughing kookaburra

In groups of the cooperatively breeding laughing kookaburra(Dacelo novaeguineae), offspring sex varied with the type ofsocial group and with hatch rank. Groups with female helpers,especially if all helpers were female, had male-biased clutchand fledging sex ratios. Groups without female helpers (unassistedpairs or male-only helpers) had female-biased clutch and fledgingsex ratios. Breeding females responded facultatively to increasesin the number of female helpers in their group by producingmore male eggs. These biases may occur if breeding femalestry to limit the number of daughters recruited into their groupbecause unlike male helpers, female helpers depress the breedingsuccess of their parents. Across all nests, two-thirds of first-hatchedyoung were male, two-thirds of second-hatched young were female, and the sex ratio of third-hatched young was even. Hatch ranksex ratios also varied dramatically between different typesof social groups, from 16.7% for second-hatched nestlings ofunassisted pairs to 100% for first-hatched nestlings of groupswith only female helpers. A corollary of the relationship betweenhatch rank and sex was that hatching sex sequences were distributed nonrandomly: all groups avoided hatching a daughter first followedby a son (FM). Sibling competition is aggressive and sometimesfatal. Since females grow to be 15% larger than males the hatchingsequence of sexes could affect nestling growth and mortality.However, an exhaustive analysis found little evidence thatgrowth or survival of males was compromised if hatched aftera sister. The small number of FM sequences may only have occurredin nests that were able to ameliorate any negative consequences.Alternatively, when clutch size is small and fledging successunpredictable because of brood reduction, the preferred broodsex ratio may be contingent on the number of fledged young,making it advantageous to order the sexes in the brood.     

Sex ratio in relation to timing of breeding, and laying sequence in a dimorphic seabird

When the cost of rearing sons and daughters differs and the subsequent survival and reproductive success of one sex is more dependent than the other, on the amount of parental investment, adult females tend to produce more chicks of the more dependent sex if the females are in good condition themselves. One method of varying the total investment in each sex is through modifying the sex ratio of offspring produced. This study shows that in broods of European Shags Phalacrocorax aristotelis , the sex ratio varied with laying date. Presumably in this species, the lifetime reproductive success of males is more dependent on the level of parental investment. Early breeders are in better condition, the brood sex ratio of early broods was male biased (0.63), while that of late broods was female biased (0.36). The overall difference in sex ratio found between early and late nests could be attributed to manipulation of sex in the first laid egg. In early broods, 77% of the first hatched chicks were male but only 30% of the first hatched chicks in late broods were male. The sex combination of the first two chicks in a brood significantly affected growth as measured by asymptotic mass.