Preferential parental investment in daughters over sons

Female-biased parental investment is unusual but not unknown in human societies. Relevant explanatory models include Fisher’s principle, the Trivers-Willard model, local mate and resource competition and enhancement, and economic rational actor models. Possible evidence of female-biased parental investment includes sex ratios, mortality rates, parents’ stated preferences for offspring of one sex, and direct and indirect measurements of actual parental behavior. Possible examples of female-biased parental investment include the Mukogodo of Kenya, the Ifalukese of Micronesia, the Cheyenne of North America, the Herero of southern Africa, the Kanjar of south Asia, the Mundugumor of New Guinea, contemporary North America, and historical Germany, Portugal, and the United States. Lee Cronk is Assistant Professor of Anthropology at Texas A&M University, College Station, Texas. His main research interests are in human behavioral ecology, reproductive strategies, and East African hunter-gatherers and pastoralists.     

Estimating relative parental investment in sons versus daughters

Fisher proposed that natural selection would adjust the population sex ratio so that parental expenditure on sons equals expenditure on daughters. Thus if two daughters can be produced for every son, the Fisherian equilibrium is ? sons and ? daughters. The relative cost of a son versus a daughter is necessarily manifested in the trade-off between family size and sex ratio, and we offer a method to estimate this trade-off from data on family compositions. Simulation studies indicate that the method works well in some cases but not others. Application of the method to data on a polychaete suggests that sons are much costlier than daughters; the observed sex ratio in fact significantly favored daughters, but not to the extreme predicted by our measure of differential cost.     

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.     

Mothers that produce sons and daughters are genetically different in red deer

Sex ratio theory, and in particular Fisher principle, assumes parental control over the sex of offspring through the action of autosomal genes with Mendelian segregation. In spite of the importance of Fisher's principle in evolutionary biology, the number of studies looking for possible loci involved in sex ratio bias is, at best, very low. Newly developed genetic tools frequently allow evolutionary biologists to manage genetic data. Here we encourage the application of association tools to databases that include genetic information for autosomal loci and offspring sex to improve our knowledge on sex ratio evolution. As an example we use microsatellite markers to scan autosomal chromosomes and look for linked genetic regions associated with offspring sex in red deer (Cervus elaphus). We found a microsatellite marker (CelJP38) mapped in chromosome 27 for which females producing sons and daughters were genetically different. To the best of our knowledge, this is the first study that shows a genetic signal that points out an association between mother genotype and offspring sex in natural populations of a mammal.     

Parental preference for sons and daughters in a Western industrial setting: evidence and implications

This paper considers whether sex composition of existing children in Australian families is an important factor in parity progression. Using census data from 1981, 1986, 1991, 1996 and 2001, women are linked with their co-resident children, allowing investigation of family sex composition and its changing impact over time on the propensity to have another child. The study finds that parents are much more likely to have a third and fourth birth if existing children are all of the same sex, indicating a strong preference for children of both sexes. This increased propensity has added around three per cent to the fertility of recent cohorts. The paper concludes with a discussion of the potential impact of sex-selection technologies on fertility. The authors argue that future widespread use of reliable sex-selection technologies might act to increase fertility in the short term, but would lead to a long-term reduction in fertility.     

Individual mares bias investment in sons and daughters in relation to their condition

The Trivers-Willard hypothesis (TWH) predicts that a mother will treat a son or daughter differently depending on her ability to invest and the impact of her investment on offspring reproductive success. Although many studies have investigated the hypothesis, few have definitively supported or refuted it because of confounding factors or an inappropriate level of analysis. We studied maternal investment in sons and daughters in feral horses, Equus caballus, which meet the assumptions of the TWH with a minimum of confounding variables. Population level analyses revealed no differences in maternal behaviour towards sons and daughters. When we incorporated mare condition, we found that sons were more costly to mares in good condition, whereas daughters were more costly to mares in poor condition, although no differences in maternal behaviour were found. However, since the TWH makes predictions about individual mothers, we examined investment by mares who reared both a son and a daughter in different years of the study. Mares in good condition invested more in their sons in terms of maternal care patterns, costs to maternal body condition and costs to future reproduction. Conversely, mares in poor condition invested more in daughters. Therefore, with an appropriate level of analysis in a species in which confounding variables are minimal, the predictions of the Trivers-Willard hypothesis are supported. Copyright 2000 The Association for the Study of Animal Behaviour.     

Mechanisms governing sex-ratio variation in dioecious Rumex nivalis

Sex ratios of flowering individuals in dioecious plant populations are often close to unity, or are male biased owing to gender-specific differences in flowering or mortality. Female-biased sex ratios, although infrequent, are often reported in species with heteromorphic sex chromosomes. Two main hypotheses have been proposed to account for female bias: (1) selective fertilization resulting from differential pollen-tube growth of female- versus male-determining microgametophytes (certation); (2) differences in the performance and viability of the sexes after parental investment. Here we investigate these hypotheses in Rumex nivalis (Polygonaceae), a European alpine herb with female-biased sex ratios in which females possess XX, and males XY1Y2, sex chromosomes. Using field surveys and a glasshouse experiment we investigated the relation between sex ratios and life-history stage in 18 populations from contrasting elevations and snowbed microsites and used a male-specific SCAR-marker to determine the sex of nonflowering individuals. Female bias among flowering individuals was one of the highest reported for populations of a dioecious species (mean female frequency = 0.87), but males increased in frequency at higher elevations and in the center of snowbeds. Female bias was also evident in nonflowering individuals (mean 0.78) and in seeds from open-pollinated flowers (mean 0.59). The female bias in seeds was weakly associated with the frequency of male flowering individuals in populations in the direction predicted when certation occurs. Under glasshouse conditions, females outperformed males at several life-history stages, although male seeds were heavier than female seeds. Poor performance of Y1Y2 gametophytes and male sporophytes in R. nivalis may be a consequence of the accumulation of deleterious mutations on Y-sex chromosomes.     

Polyandry produces sexy sons at the cost of daughters in red flour beetles

Female mating with multiple males within a single fertile period is a common phenomenon in the animal kingdom. Female insects are particularly promiscuous. It is not clear why females mate with multiple partners despite several potential costs, such as expenditure of time and energy, reduced lifespan, risk of predation and contracting sexually transmitted diseases. Female red flour beetles (Tribolium castaneum) obtain sufficient sperm from a single insemination to retain fertility for several months. Nonetheless they copulate repeatedly within minutes with different males despite no direct fitness benefits from this behaviour. One hypothesis is that females mate with multiple partners to provide indirect benefits via enhanced offspring fitness. To test this hypothesis, we compared the relative fitness of F(1) offspring from females mated with single males and multiple males (2, 4, 8, or 16 partners), under the condition of relatively high intraspecific competition. We found that a female mating with 16 males enhanced the relative fitness of F(1) males (in two out of three trials) but reduced F(1) females' fitness (in two independent trials) in comparison with singly mated females. We also determined whether several important fitness correlates were affected by polyandry. We found that F(1) males from mothers with 16 partners inseminated more females than F(1) males from mothers with a single partner. The viability of the eggs sired or produced by F(1) males and females from highly polyandrous mothers was also increased under conditions of low intra-specific competition. Thus, the effects of polyandry on F(1) offspring fitness depend on environmental conditions. Our results demonstrated a fitness trade-off between male and female offspring from polyandrous mothers in a competitive environment. The mechanisms and biological significance of this unique phenomenon are discussed.     

Diploid males sire triploid daughters and sons in the parasitoid wasp Cotesia vestalis

In the Hymenoptera, males develop as haploids from unfertilized eggs and females develop as diploids from fertilized eggs. In species with complementary sex determination (CSD), however, diploid males develop from zygotes that are homozygous at a highly polymorphic sex locus or loci. We investigated mating behavior and reproduction of diploid males of the parasitoid wasp Cotesia vestalis (C. plutellae), for which we recently demonstrated CSD. We show that the behavior of diploid males of C. vestalis is similar to that of haploid males, when measured as the proportion of males that display wing fanning, and the proportion of males that mount a female. Approximately 29% of diploid males sired daughters, showing their ability to produce viable sperm that can fertilize eggs. Females mated to diploid males produced all-male offspring more frequently (71%) than females mated to haploid males (27%). Daughter-producing females that had mated to diploid males produced more male-biased sex ratios than females mated to haploid males. All daughters of diploid males were triploid and sterile. Three triploid sons were also found among the offspring of diploid males. It has been suggested that this scenario, that is, diploid males mating with females and constraining them to the production of haploid sons, has a large negative impact on population growth rate and secondary sex ratio. Selection for adaptations to reduce diploid male production in natural populations is therefore likely to be strong. We discuss different scenarios that may reduce the sex determination load in C. vestalis.     

Maternal effects influence the sexual behavior of sons and daughters in the zebra finch

Individual differences in sexual behavior have received much attention by evolutionary biologists, but relatively little is known about the proximate causes of this variation. We studied the quantitative genetics of male and female sexual behavior of captive zebra finches and found surprisingly strong maternal effects (differing between individual mothers) on the aggressiveness and song rate of sons and on the daughters' mating preferences for these male traits. We also found that daughters differed in their choosiness during mate-choice experiments depending on whether they originated from eggs produced early or late within the laying sequence of a clutch. Because this effect of laying order occurred independently of hatching order in cross-fostered broods, it must have been caused by consistent within-mother variation in maternal effects transmitted through the egg. Our findings raise the question whether these maternal effects might represent strategic programming of offspring behavior in response to the environment experienced by mothers or whether they are merely nonadaptive byproducts of developmental processes.     

Spacer 2 region and 5S rDNA variation of Wolbachia strains involved in cytoplasmic incompatibility or sex-ratio distortion in arthropods

Bacteria in the genus Wolbachia are widespread in arthropods and can induce sex-ratio distortion or cytoplasmic incompatibility in their hosts. The phylogeny of Wolbachia has been studied using 16S rDNA and the cell cycle gene ftsZ, but sequence variation of those genes is limited. The spacer 2 region (SR2) was amplified to determine whether this region would improve phylogenetic resolution. The SR2 of Wolbachia is 66 bp long, shows higher variation than ftsZ and has very low homology with closely related bacteria. Due to the small length of SR2 of Wolbachia, little phylogenetic information could be retrieved.     

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.     

Internest sex-ratio variation and male brood survival in the ant Pheidole pallidula

Sex allocation in social insects has become a general modelin tests of inclusive fitness theory, sex-ratio theory, andparent-offspring conflict. Several studies have shown that colonysex ratios are often bimodally distributed, with some coloniesproducing mainly females and others mainly males. Sex specializationmay result from workers assessing their relatedness to malebrood versus female brood, relative to the average worker-relatednessasymmetry in other colonies of their population. Workers thenadjust the sex ratio in their own interest This hypothesis assumesthat workers can recognize the sex of the brood in their colonyand selectively eliminate males. We compared the primary sexratio (at the egg stage) and secondary sex ratio (reproductivepupae and adults) of colonies in the ant Pheidole pallidula.There was a strong bimodal distribution of secondary sex ratios,with most colonies producing mainly reproductives of one sex.In contrast, there was no evidence of a bimodal distributionof primary sex ratios. The proportion of haploid eggs producedby queens was 0.35 in early spring and decreased to about 0.1in summer. Male eggs also were present in virtually all fieldcolonies sampled in July, although eggs laid at this time ofyear never give rise to males. All male brood is, therefore,selectively eliminated beginning in July and continue to beeliminated through the rest of the year. Finally, the populationsex-ratio investment was female-biased. Together, these resultsare consistent with the hypothesis that workers control thesecondary sex ratio by selectively eliminating male brood inabout half the colonies, perhaps those with high relatednessasymmetry.[Behav Ecol 7: 292–298 (1996)]     

Does the differential cost of sons and daughters lead to sex ratio adjustment in great frigatebirds Fregataminor?

Sex allocation theory predicts that if benefits of producing sons and daughters differ and outweigh the costs of sex ratio adjustment, parents should produce more of the offspring that provide them with greater fitness. Potential benefits may be more likely to outweigh costs where sexual size dimorphism and, in birds, single‐egg clutches exist. Great frigatebirds Fregataminor are seabirds in which females are larger than males and clutch size is one egg. In our study population, sexual size dimorphism develops primarily during the period of complete juvenile dependence on parental care, consistent with a higher cost of producing daughters than sons. Over the course of the 1998 breeding season there was a shift from early season prevalence of daughters to late‐season prevalence of sons. Variation in food availability at time of egg laying, as indexed by sea surface temperature (SST), was a strong predictor of offspring sex in 1998. In contrast, SST in 2003 was not a predictor of offspring sex, nor was there a seasonal shift in the hatching sex ratio, despite a seasonal shift in SST. Besides food availability, we tested two additional factors in 2003 that could explain sex ratio adjustment in relation to the cost of reproduction. Offspring sex in 2003 was not related to natural or experimentally induced variation in maternal body condition; pre‐laying food supplements raised the body condition of females at the time of egg laying but did not affect offspring sex or egg mass. In addition, offspring sex was not predicted by the length of maternal telomere restriction fragments (TRFs), an index of age and possibly of reproductive experience. Broad confidence intervals on effect size suggest that undetected effects of maternal condition on offspring sex ratio could easily exist, but confidence intervals were narrower on the non‐significant effects of SST and TRF length on offspring sex ratio. The cause of different seasonal patterns of hatching sex ratio and different SST effects in 1998 and 2003 is unclear.     

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.     

Nuclear sex-determining genes cause large sex-ratio variation in the apple snail Pomacea canaliculata

Evolutionary maintenance of genetic sex-ratio variation is enigmatic since genes for biased sex ratios are disadvantageous in finite populations (the "Verner effect"). However, such variation could be maintained if a small number of nuclear sex-determining genes were responsible, although this has not been fully demonstrated experimentally. Brood sex ratios of the freshwater snail Pomacea canaliculata are highly variable among parents, but population sex ratios are near unity. In this study, the effect of each parent on the brood sex ratio was investigated by exchanging partners among mating pairs. There were positive correlations between sex ratios of half-sib broods of the common mother (r = 0.42) or of the common father (r = 0.47). Moreover, the correlation between full-sib broods was very high (r = 0.92). Thus, both parents contributed equally to the sex-ratio variation, which indicates that nuclear genes are involved and their effects are additive. Since the half-sib correlations were much stronger than the parent-offspring regressions previously obtained, the variation was caused by zygotic sex-determining genes rather than by parental sex-ratio genes. The number of relevant genes appears to be small.     

Simultaneous failure of two sex-allocation invariants: implications for sex-ratio variation within and between populations

Local mate competition (LMC) occurs when male relatives compete for mating opportunities, and this may favour the evolution of female-biased sex allocation. LMC theory is among the most well developed and empirically supported topics in behavioural ecology, clarifies links between kin selection, group selection and game theory, and provides among the best quantitative evidence for Darwinian adaptation in the natural world. Two striking invariants arise from this body of work: the number of sons produced by each female is independent of both female fecundity and also the rate of female dispersal. Both of these invariants have stimulated a great deal of theoretical and empirical research. Here, we show that both of these invariants break down when variation in female fecundity and limited female dispersal are considered in conjunction. Specifically, limited dispersal of females following mating leads to local resource competition (LRC) between female relatives for breeding opportunities, and the daughters of high-fecundity mothers experience such LRC more strongly than do those of low-fecundity mothers. Accordingly, high-fecundity mothers are favoured to invest relatively more in sons, while low-fecundity mothers are favoured to invest relatively more in daughters, and the overall sex ratio of the population sex ratio becomes more female biased as a result.