Litter Sex Ratio Research Articles

Pregnancy in female house mice exposed to urinary chemosignals from other females.

Seven experiments were performed to investigate pregnancy termination, urinary chemosignals, and litter sex ratio variation in female house mice. Experiments tested the effects of urine from adult and prepubertal females, housed individually or in groups, on successful insemination and litter production by females treated at different times and for different periods during the 3 weeks before mating and during gestation. Treatment of females with urine from adult females housed eight per cage or with urine pooled from eight adult females housed individually for 2 or 3 weeks before mating resulted in fewer successful pregnancies and significantly more female-biased litters. Treatment with urine from adult or prepubertal females housed eight per cage or with urine pooled from eight mice housed individually for the first 6 days of gestation or throughout pregnancy resulted in a significant increase in the rate of pregnancy termination. These treatments resulted in lower body weights at birth and slower growth rates in all males and in some females. Puberty was delayed in female progeny from urine-treated dams in five of seven experiments, and these young females attained first oestrus at greater mean body weights than mice in other treatments. These findings indicate that, in mice, at high population density, communication via a urinary chemosignal can alter reproduction in recipient females. Availability of, and competition for, resources such as food would be greater at higher densities, possibly lowering the probability of reproductive success. Pregnancy termination and delays in reproduction and attainment of sexual maturity might lead to greater successful reproduction at a later time.

Factors affecting the number of teats in pigs.

The factors that affect the number of teats in pigs are of interest for both biological and practical reasons. Previous work indicates that there is a genetic component, principally from the dam. The proportion of males in a litter appears to be related to the anogenital distance of the gilts in the litter, possibly as a result of the intrauterine position effect. The present study investigated whether litter size, litter sex ratio, anogenital distance, crown-rump length, distance from base of skull to base of tail, and the number of teats on the dam and boar affected the number of teats on gilts. Stepwise multiple regression on litter mean values (adjusted r2 = 0.178) indicated that two factors were significant: the number of teats on the dam (standard coefficient 0.311) and the proportion of males in the litter (standard coefficient -0.282). A greater number of teats on the dam and a lower proportion of males in the litter resulted in a greater number of teats on the gilt. When the analysis was run using individual gilts as the independent units (adjusted r2 = 0.073), the number of teats on the dam (standard coefficient 0.207), the proportion of males in the litter (standard coefficient -0.135), and the weaning weight of the gilt (standard coefficient 0.083) were all significant predictors of the number of teats. This evidence suggests that teat number in female pigs is related to the proportion of males in the litter.

Litter sex ratios in a food-supplemented population of Peromyscus mexicanus

We examined the tertiary sex ratio of litters in a wild population of the tropical mouse Peromyscus mexicanus for evidence of facultative adjustment of the sex ratio as a function of (i) three maternal characteristics, mass at conception, litter parity, and access to a food supplement, and (ii) rainfall and temperature around the time of early gestation and around the time of birth. We examined unreduced litters (litters that had not experienced losses during gestation or lactation, usually 3 pups) separately from litters of all sizes in order to distinguish between prenatal (unreduced litters) and postnatal (all litters) shifts in litter composition. We also examined a sample of litters that were enumerated at birth for further evidence of prenatal adjustment of the sex ratio. None of the independent variables were significant predictors of the frequency of male pups. Furthermore, we found no evidence that litters of any size deviate from a sex ratio of 1.0, whether enumerated at birth or at weaning. Sex-ratio shifts occur in other species of Peromyscus, but P. mexicanus has a low reproductive potential, and adjustment of litter composition may not occur because such a strategy is too costly and too risky.

The effect of an improved man–animal relationship on sex ratio in litters and on growth and behaviour in cubs among farmed silver fox ( Vulpes vulpes)

Earlier experiments indicate that silver foxes' fear of humans can be reduced by humans offering them food titbits. Sex ratio, cub growth and behaviour were examined in litters produced by multiparous silver fox vixens that had been given a titbit twice a week during pregnancy (G1, N=14) or received the same amount of human contact without any titbit (G2, N=14). The cubs were tested in an open field (1.15×1.15 m square area divided into a 5×5 square grid) at 30 days of age, when they were in the early stages of primary socialisation. Cub activity was recorded (number of grid lines crossed [Lc] during 3 min). There was no treatment-related difference in number of cubs born or cubs weaned at 49 days (4.9±0.3 and 4.1±0.4 vs. 4.8±0.5 and 3.8±0.4 for G1 and G2, respectively; NS). However, G1 vixens delivered a significantly higher proportion of male cubs than G2 vixens (64% vs. 51%, p<0.05; G1:3.1±0.4 male cubs, 1.8±0.3 female cubs; G2:2.5±0.4 male cubs, 2.3±0.3 female cubs). Female cubs from G1 vixens were more active in the open field (G1:51.4±4.8 Lc, G2:34.2±4.7 Lc, p<0.05) and heavier (49 days old, G1:1660±42 g, G2:1491±40 g, p<0.01) than the female G2 cubs. No significant differences in activity or live weight were found for male cubs (activity: G1:46.4±3.4 Lc, G2:37.1±4.3 LC, NS; weight 49 days old: G1:1716±29 g, G2:1729±37 g, NS). Reduced fear of humans during pregnancy affected the sex ratio in the litter as well as the growth and activity of female cubs in the silver fox.

Timing of Mating, Developmental Asynchrony and the Sex Ratio in Mice

Krackow, S. and P. S. Burgoyne. Timing of mating, developmental asynchrony and the sex ratio in mice. PHYSIOL BEHAV 63(1): 81–84, 1998.—According to the developmental asynchrony hypothesis, changing the time of mating within the estrous cycle could alter the interval between completion of blastocyst development and uterine responsiveness for implantation. This may then lead to sex ratio skews in animals that exhibit sex-differential blastocyst development, because uterine stage may now benefit either slow (female) or fast (male) developing blastocysts. To test this hypothesis, the responses of two strains of mice to altered mating dynamics were compared. In a strain that exhibits higher male than female blastocyst developmental rates, sex ratios became significantly female-biased when mated late during the estrous cycle as opposed to early mating. However, timing of mating did not affect sex ratios in a strain with synchronous development of male and female preimplantation embryos. Hence, it is concluded that developmental asynchrony between male and female blastocysts on the one hand, and blastocysts and uterus on the other, are indeed responsible for the effect of timing of mating on litter sex ratios in mice.

Effects of mating dynamics and crowding on sex ratio variance in mice.

Mating units of six virgin females and one adult stud male were established to test for the effects of timing of mating and crowding of pregnant females on litter sex ratios in mice. Females either copulated during periods when no other female of the mating unit copulated simultaneously (single mating condition) or when more than one female copulated (multiple matings condition). Two crowding conditions were imposed on the animals: the females of 14 mating units were placed into individual cages after mating (isolated condition), while females of the other 13 mating units remained in the original group until shortly before littering (crowded condition). Sex ratio variance did not deviate from random expectation in litters arising from the multiple matings periods. However, in litters arising from single mating periods, extreme sex ratios were found significantly less frequently than expected by chance. Higher sex ratio variance in litters arising from multiple matings periods is attributed to the timing of mating being at higher variance under this condition, which is known to affect sex ratios in other rodents. Crowding significantly reduced sex ratio variance further. Reduced sex ratio variance under single mating and crowded conditions is speculated to follow from competition for resources between preimplantation embryos, which may be further increased by stressful effects of crowding. Loss of embryos after implantation appeared not to be responsible for the above effects.

Skewed offspring sex ratios and sex composition of twin litters in Serengeti spotted hyaenas ( Crocuta crocuta) are a consequence of siblicide

Long-term data on the sex ratio among offspring and sex composition of litters in a population of several hundred individually known spotted hyaenas in the Serengeti National Park, Tanzania are presented. Females produced singleton or twin litters. The overall sex ratio (proportion of males) was unbiased at 0.52 ( n = 318) but masked significant deviations in opposite directions in litters of different size. Sex ratio in singleton litters was female biased at 0.43 ( n = 91 individuals, p = 0.07). The sex ratio in twin litters was significantly ( P < 0.05) male-biased at 0.56 ( n = 228 individuals); there were significantly too many mixed-sex and too few all-female twin litters. Three hypotheses are considered that may explain these sex ratio biases: (i) the primary sex ratio may be skewed, (ii) cub mortality may be female-biased, leading to the loss of more females than males, or (iii) the biases are due to siblicide. The first two hypotheses predicted the same sex ratio biases for both singleton and twin litters, while the third hypothesis predicted opposite trends for singleton and twin litters. The results are inconsistent with the two first hypotheses but support the third. The study suggests that the lack of all-female twin litters and the female bias amongst singletons is due to a higher incidence of siblicide in all-female twin litters than among mixed-sex or all-male twin litters. Siblicide is the major source of post-natal sex ratio biases to the age of independence in this population.

Conception failure in swine: importance of the sex ratio of a female's birth litter and tests of other factors.

Failure of gilts and sows to conceive when they are mated is a potentially serious economic cost for swine producers. In Exp. 1, we determined that anogenital distance of newborn gilts is related to the proportion of males in the litter (P < .001). Gilts from litters with more males have larger anogenital distances (mean = 8.0 +/- .2 mm); those from litters with low proportions of males have smaller anogenital distances (mean = 5.7 +/- .1 mm). In Exp. 2, we examined the effect of birth litter sex ratio of sows and gilts on reproductive performance using a 13-yr database of breeding and litter data. Gilts that failed to become pregnant on the first breeding attempt came from litters with significantly higher proportions of males than gilts that successfully conceived on the first breeding attempt. Overall, female swine were significantly more likely to exhibit lower rates of successful breeding during their first four breeding attempts if they had been born in a male-biased litter. These results have implications for swine producers deciding which gilts to keep and which to market. Given the higher probability of reproductive problems for gilts from litters of 12 or more pigs with 67% or more males, these females should likely become market hogs. Sow's age, mode of insemination, and the number of insemination attempts at an estrus period, but not season, can affect successful breeding.

Male sexual rest affects litter sex ratio of newborn Norway rats

Associations between male sexual rest and litter sex ratio have been reported in Norway rats, Rattus norvegicus, but the direction of the effect has been inconsistent. Female rats were paired with either a male that had copulated to satiety three weeks previously or a male that had copulated within the previous four days. Females were paired during both a cycling oestrus and a postpartum oestrus. Sex-ratio biases were only observed in litters conceived during a cycling oestrus. Litters sired by rested males had higher sex ratios than litters sired by unrested males. This relationship was mediated by differences in the timing of mating events, including length of post-ejaculatory interval and the time at which effective mating was completed. Sex ratio was negatively associated with time of mating completion, replicating earlier findings. Only litters that had fewer pups at birth than at implantation showed the relationship between sex ratio and rest-mediated mating behaviour. These litters were not smaller than litters without loss, however. Post-implantation loss was more likely to occur when uterine horns were crowded, suggesting that this type of sex-ratio biasing occurs in the context of adaptive litter reduction. This association between paternal behaviour, paternal condition and offspring sex ratio prompts the hypothesis that females use the timing of mating behaviour to evaluate heritable traits that might affect male mating success, and then adjust offspring sex ratio to maximize offspring reproductive success.

Reproductive output, costs of reproduction, and ecology of the smooth snake, Coronella austriaca, in the eastern Italian Alps.

A 5-year mark-recapture study of smooth snakes (Coronella austriaca) in the Carnic Alps (1100 m above sea level) of north-eastern Italy provided extensive information on the biology and life-history of these small viviparous snakes. Offspring were relatively large (mean=15 cm total length, 2.9 g) when they were born in late summer, and females grew to maturity (44 cm, 50 g) in approximately 4 years. Larger neonates retained their size advantage for at least 12 months, but did not have a higher probability of survival. Although sexual size dimorphism (at birth and at mean adult body sizes) was minor, the sexes differed significantly in several respects. Females grew faster than males during juvenile life, and adult females diverged in dietary habits from the rest of the population. Whereas juveniles (of both sexes) and adult males fed primarily on lizards, larger females shifted to feeding less frequently, but taking larger prey (mammals and snakes). Reproductive output increased strongly with maternal body size: larger females reproduced more frequently, produced larger litters of larger neonates, had higher relative clutch masses (RCMs), and had a lower proportion of stillborn off-spring. Most females produced a litter every 2nd or 3rd year. We did not detect significant year-to-year variation in reproductive traits over the 5 years of our study. Females were consistent from one litter to the next in several traits (e.g., litter sizes, offspring sizes and shapes, proportions of stillborn neonates, RCMs), but this consistency was due to differences in body size among females rather than to size-independent maternal effects. Overall litter sex ratios averaged 50/50, but sex ratios tended to be more male-biased in litters that were unusually large relative to maternal body size, and in litters containing a high proportion of stillborn offspring. "Costs" of reproduction appear to be high in this population, in terms of both energy allocation and risk. Reproduction reduced growth rates, and females that recovered condition more quickly in the year after reproduction were able to reproduce again after a briefer delay. Mortality was highest in reproducing females with high RCMs, and in females that were very emaciated after parturition. The marked increase in reproductive output with increasing maternal body size in C. austriaca may reflect a reduction in "costs" as females grow larger, and the dietary shift to larger prey may enhance the rate that females can accumulate energy for reproduction.

Increased secondary sex ratios in golden hamster litters sired by males without coagulating glands and seminal vesicles

In golden hamsters, although bilateral ablation of paternal coagulating glands (CGX) and seminal vesicles (SVX) did not affect fertility, a higher number of male pups were born. The present study aimed at determining whether this male-biased sex ratio was due to an imbalance of fertilization by X and Y chromosome-bearing sperms or whether it was the consequence of a sex-related differential survival of embryos. The sex of embryos sired by sham-operated (SH) controls or males subjected to bilateral ablation of ampullary glands (AGX), CGX and SVX was determined from chromosomal spreads at 10 h post coitum and 10 days post coitum. The primary sex ratio of of the SH group did not deviate from the hypothetical sex ratio of 1:1. The sex ratios of zygotes from the three experimental groups did not differ from that of the controls. However, by mid gestation, the sex ratio was significantly higher in the SVX group (P < 0.05) and the CGX group (P < 0.005). The absence of secretions from the ampullary gland, coagulating gland and seminal vesicle had no effect on the primary sex ratio, thus these glands did not appear to affect fertilization by the X and Y chromosome-bearing sperm. The increased secondary sex ratios observed in the SVX and CGX groups were due to the preferential survival of males.

Variation in Sex Ratios of Offspring in Wild Bushy-Tailed Woodrats

We investigated the effects of maternal weight and age and density of breeding females on sex ratio (percentage of males) in litters of wild bushy-tailed woodrats ( Neotoma cinerea ), a sexually dimorphic rodent. Sex ratios in full-sized litters (i.e., those that had not likely experienced mortality during gestation or lactation) were unaffected by experimentally reduced densities of females, nor did they differ between litters born to yearling and adult (≥2 years) mothers. However, sex ratios in litters were strongly correlated ( R = 0.71, P = 0.0001) with prebreeding body weight in adult mothers, suggesting that adult woodrats adjust sex ratios in litters at conception or early gestation in relation to maternal condition. Although yearling mothers did not appear to adjust prebirth sex ratios, postbirth loss was more strongly male-biased in litters born to yearling mothers than in those born to adults, and we suggest that yearlings may adjust sex ratios during the investment period from birth to weaning.

Influence of the natal environment on dispersal of white-footed mice

We explored the relationship between several aspects of the natal environment and dispersal distances of white-footed mice, Peromyscus leucopus, in a 2-ha oak/hickory woodlot northeast of Bowling Green, Ohio, from 1991 to 1993. Litters of mice in nestboxes were marked at an early age. We evaluated litter size, the number of males and females in the litter, litter sex ratio, weanling survival to adulthood, and mother's parity as proximate factors that might affect dispersal. Dispersal was quantified as the straight-line distance between the mother's center of activity and that of her adult offspring. Of 401 mice from 82 litters, 78 (19.5%) were recaptured as adults. Males dispersed significantly farther than females. Females from small litters dispersed shorter distances than females from median or large litters. Females also dispersed farther with increasing numbers of male siblings. However, the proportion of males in the litter was not related to dispersal distance of either sex. Males with two or more sisters dispersed farther than did males with fewer than two sisters. Males from their mother's first litter dispersed farther than males from subsequent litters; however, the presence or absence of the mother at the time of dispersal was not related to male dispersal distance. Our results suggest that inbreeding avoidance between siblings may lead to male-biased dispersal, and that interactions between siblings may be more important than interactions with the mother in determining dispersal distances.

Root Voles: Litter Sex Ratio Variation in Fragmented Habitat

1. Litter sex ratio variation in enclosed populations of two strains of root voles originating from northern and southern Norway was studied in experimentally fragmented habitats during 2 years (1990 and 1991) in the period early July-mid October. 2. Three fragmentation patterns differing with respect to habitat fragment size and interfragment connectivity (corridors) were colonized by voles from either strain in each of the 9 years ; yielding two population replicates per strain and fragmentation pattern. Litter affiliation of weanlings was decided from a combination of trapping data, marking of lactating mothers with fluorescent powder and marking of nestlings. 3. Habitat fragmentation had no consistent influence on weanling sex ratio at the population level. However, within populations of both strains, mothers inhabiting a habitat fragment alone produced more female-biased litters than those sharing a fragment with other reproductive females. 4. For the south Norwegian strain, large mothers produced more female-biased litters than small mothers. The southern strain had an overall female-biased weanling sex ratio the first year, probably because reproductive females were generally heavier in 1990 than in 1991. 5. The results are consistent with hypotheses predicting that females should adjust the litter sex ratio according to resource availability and social environment at a local scale, as well as to their own competitive ability. It is argued that adaptive sex ratio variation in Microtus is more probably due to spatial variability of fitness returns from daughters than from sons, because females are the philopatric sex and compete at a smaller spatial scale than males.

A gerbil dam's fetal intrauterine position affects the sex ratios of litters she gestates

The vaginally delivered litters of gerbil dams that, in utero, occupied intrauterine positions between two males fetuses (2M females) contain a greater proportion of sons than do the vaginally delivered litters of gerbil dams that were gestated between two female fetuses (2F females). This difference in the sex ratios of litters delivered vaginally by 2M and 2F gerbils might reflect sex-biased differences in perinatal mortality in the litters of 2M and 2F dams. However, the results of the present experiment, in which gerbil litters were delivered by caesarian section from females that developed in 2M and 2F intrauterine positions, demonstrated unequivocally that 2M female gerbils gestate male-biased litters, whereas 2F female gerbils gestate female-biased litters.

Maternal social status and birth sex ratio in domestic pigs: an analysis of mechanisms

In support of the Trivers & Willard model of adaptive variation in birth sex ratio, recent research showed that high-ranking female domestic pigs, Sus scrofa, gave birth to a greater proportion of sons than low-ranking females. Differences in maternal nutritional status caused by differential access to food of high- and low-ranking females, or differences in adrenal activity as the result of stress experienced during agonistic encounters are two possible mechanisms underlying these findings. This study examined the role that these mechanisms may play, and further investigated the relationship between social status and birth sex ratio in the pig, not only within, but also across pregnancies. The reproductive performance of a group of 37 female pigs was recorded across four pregnancies. Social status and adrenal activity of individuals were assessed during the first and fourth pregnancies. Within each pregnancy, there was no relationship between social status and birth sex ratio. Despite cross-pregnancy consistency in social status, there was no consistency in the sex ratios of the females' consecutive litters. However, high-ranking females produced significantly fewer males across all four pregnancies. There was no linear relationship between a female's social status and adrenal activity, and no evidence that adrenal activity was related to subsequent birth sex ratio. Maternal weight gain during pregnancy (an indicator of nutritional status) was unrelated to birth sex ratio. Data from a study of maternal nutrition in pigs also failed to show a clear relationship between nutritional status and birth sex ratio. Differences between the findings of the present and previous studies are discussed from functional and causal perspectives.

Mother's prior intrauterine position affects the sex ratio of her offspring in house mice.

Sex ratio alterations related to environmental factors occur in several mammals, but no mechanism has been identified to explain the adjustment. Intrauterine position (IUP) may provide the context in which such alterations occur. Previous studies on house mice and gerbils reveal that the position of a fetus in the uterus in relation to the sex of its neighbors influences its later anatomy, physiology, and behavior. The anogenital distance (AGD) of females located between two males (2M) is longer than that of females not between two males (OM). We have found that the IUP, as determined by cesarean section and by an index of the AGD, correlates with the sex ratio of the litters produced by female mice. The sex ratio of the first litter born to 2M females was 58% males, for 1M females was 51% males and for OM females was 42% males. The effect on sex ratio continues into the second litter. The number of pups produced by mothers of different IUPs in her first two litters did not differ, suggesting that the sex ratio adjustment occurs prior to parturition. These results provide a basis for the natural variability observed in sex ratios of litter-bearing mammals and suggest that one or more intrauterine mechanisms may be responsible for environmentally related sex ratio alterations.

Performance (re-acquisition) of a water-maze task by adult meadow voles: Effects of age of initial task acquisition and in utero environment (litter sex-ratio)

Previous research in this laboratory has shown that preweaning and postweaning juvenile meadow voles, Microtus pennsylvanicus, can acquire a spatial task, the Morris water-maze task. The present study examined the influence of age of juvenile acquisition (“before weaning” (BW; Day 10 and 15 after birth) and “after weaning” (AW; Day 20 and 25 after birth)) of a spatial task on subsequent re-acquisition of the same hidden-platform spatial water-maze task. This study also compared sex differences and litter sex-ratio effects on reacquisition performance. Fifteen litters of adults were re-tested in the same water maze 6 weeks after being initially tested as juveniles. All analyses were conducted using a covariate that removed the group differences in the original task performance. Adult voles from female-biased litters, that had previously learned the task at an older juvenile age (AW), reacquired the same task faster than adults that had previously learned the task at a younger juvenile age (BW). In the adult BW group there was also a significant litter sex-ratio effect such that voles born into a female-biased litter re-acquired the task more slowly than did voles born into a male-biased litter. There were no significant sex or litter sex-ratio effects on spatial learning in the AW group. These results show that adult meadow voles can reacquire a spatial task more quickly if they initially learned the task at an older juvenile age, suggestive of a period of infantile amnesia. In addition, these results indicate that the litter sex-ratio can affect adult spatial performance, suggesting that the relative amount of androgens in utero may influence the development of sexually-dimorphic spatial ability in adulthood.

Multiple factors determine the sex ratio of postpartum-conceived norway rat litters

When Norway rat litters are nursed communally, postpartum-conceived litters born asynchronously are female biased at birth. To determine if one or more mechanisms produced this sex ratio bias, we studied litters conceived at a postpartum estrus, and systematically varied the presence or absence of a litter suckling during gestation. Four different factors biased the sex ratio of postpartum-conceived litters. Postpartum condition, implantation in a single uterine horn, and very large litter size favored the birth of female pups. The presence of suckling pups during gestation, on the other hand, brought the sex ratio up to parity. Each factor operated at or before implantation, and apparently did so asymmetrically in the two horns of the uterus. Thus, a litter's sex ratio at birth, even a sex ratio of parity, can be the result of multiple mechanisms of bias, some working in opposition to each other. Theories of sex ratio biasing must incorporate multiple mechanisms rather than focusing on single mechanisms within a given species.

Litter sex ratio variation in laboratory colonies of two geographically distinct strains of the root vole Microtus oeconomus

Litter sex ratio at birth was studied in two laboratory colonies of root voles Microtus oeconomus originating from northern and southern Norway, respectively Sex ratio was female biased in the northern (57% females), but not in the southern colony Sex seemed to be binomially distributed within litters of both colonies, and did not show consistent relationships with mother weight, litter size, parity or number of generations bred in the laboratory Both colonies originated from populations exhibiting cyclic population dynamics in the wild Thus different demography as such is unable to explain the difference in sex ratio between the two laboratory colonies Social organization has been shown to differ between the two strains of root voles both in the field and in the laboratory, but it is yet unclear whether this factor is related to the sex ratio difference documented in this laboratory study