Effect of sex ratio of the birth litter on subsequent reproductive performance of gilts.

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The production of offspring typically requires wex of resources derived from both the environment and maternal somatic reserves. As such, the availability of either of these types of resources has the potential to limit the degree to which resources are allocated to reproduction.

Theory and empirical studies have argued that mothers modify reproductive performance relative to exogenous resource availability and maternal condition by adjusting size, number or sex of offspring produced. These relationships have classically been defined relative to availability of energy sources; however, in vertebrates, calcium also plays a critical role in offspring production, as a considerable amount of calcium is required to support the development of offspring skeleton s.

We tested whether the availability of calcium influences reproductive output by providing female white-footed mice with a low-calcium or standard diet from reproductive maturity to senescence.

We then compared maternal skeletal condition and reproductive output, based on offspring mass, offspring number and litter sex ratio, between dietary treatments. Mothers on the low-calcium diet exhibited diminished skeletal condition at senescence and produced smaller and strongly female-biased litters. We show that litter condition and calcium intake can influence sex ratio and reproductive output following general theoretical models of resource partitioning litfer reproduction.

Editor: Paul A. This is an open-access sex distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. The funders had no role in study design, data collection and analysis, litger to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist. Life history theory predicts that mothers should optimize their reproductive success by partitioning resources in a manner that will afford them greatest fitness [1][2].

To this end, maternal attributes e. Specifically, the number, size and, under certain conditions, sex of offspring produced at a given time lutter be affected by these factors. Greater maternal body fat stores and greater body fat utilization by mothers in polar bears Ursus maritimus and moose Alces alces has also been correlated with greater weaning mass [7][8]. And, the availability of food is positively correlated with litter size in Prairie voles Microtus ochrogaster and Columbian ground squirrels [9][10].

Trivers and Litter [11] proposed that for polygynous species in which the reproductive success of male offspring dex more condition-dependent than that of female offspring, mothers in good condition should produce more male progeny than mothers in poor condition. In both roe deer Capreolus capreolus and reindeer Rangifer tarandusgreater maternal body mass has been associated with the production of a higher proportion of male offspring [12][13] ; however, support for the Trivers-Willard hypothesis in mammals, including subsequent studies in the aforementioned species, is generally equivocal [14][15][16][17]and has only been consistently demonstrated when maternal condition is quantified around the time of conception [18] sed, [19].

The effect of sdx condition on reproductive output has principally been examined relative to the availability of energy sources see [3][14][15][20] lifter reviews. However, sxe is best described as a measure of the functionality of cellular processes in the body, which encompasses a broad array of genetic and phenotypic components [21] that are not necessarily be associated with energy utilization.

Regarding resources required for the production of young, a substantial amount of calcium must also be partitioned to mammalian offspring to support skeletal development and mineralization.

Available calcium is traded-off between maternal skeletal stores and developing bone in their young. Thus, processes supporting maternal and offspring skeletal growth and integrity must also be considered to be vital components of condition [22][23].

Maternal bone loss during gestation and lactation has been observed in several species of mammals [24][25][26]. As such, a trade-off likely exists between maternal skeletal condition and offspring production in mammals. Small mammals may be more susceptible to this interaction for three reasons.

Second, litrer mammals possess proportionately smaller skeletons, and thus relatively smaller sex reserves, than larger mammals [36][37]. Finally, small mammals transfer relatively large amounts of calcium sex their offspring, based on high milk outputs [38] and milk calcium concentrations that are comparable to other mammals [39]. Few studies have addressed how calcium intake affects reproductive output in mammals outside of addressing offspring skeletal characteristics.

It has been shown that big brown bats Eptesicus fuscus produce larger offspring relative to maternal mass when fed a calcium supplement [40]and hypocalcemia has been associated with diminished litter size and female fertility in rats [14][41]. With regard to sex ratio, female rodents tend to produce fewer male offspring when stressed by nutritional deficiencies [14]however the potential impact of calcium deficiency on sex ratio has not been previously investigated.

Given the cost incurred by the maternal skeleton associated with offspring production, and that skeletal condition reflects both exogenous and endogenous calcium availability, we hypothesized that mammals adjust reproductive output relative to exogenous calcium availability and endogenous calcium stores in the skeleton. Specifically, we predicted that females with low litter intake and lower bone mineral content, as indicated by the architectural characteristics of bone at key sites of mobilization, would give birth to fewer or smaller young, and that the primary sex ratio of the young would be skewed toward females.

We also considered the effects of maternal age, parity, body mass, and calcium intake on factors associated with reproductive performance. White-footed mice lose bone over the course of gestation and lactation, and bone loss is intensified when mothers are consuming a low-calcium diet [42]. White-footed mice also allocate less calcium to individual offspring when dietary intake is reduced [42]thus littsr them a good model for testing the Trivers-Willard hypothesis within the context of calcium utilization.

We provided females with ad-lib water and access to one of two custom manufactured diets that differed only in calcium content modified TD. Seven females received a low-calcium diet 0. We provided females with 4—5 breeding opportunities over a lotter of 75 weeks.

We used a random number generator to select males for pairing with females and females were never paired with the same male more than once.

Males were comparable in age to the females and were maintained on the standard sex prior to pairing. Males were paired with females for 14 days, allowing for insemination but also ensuring that the males were litfer before females gave birth. Pups were counted, sexed, and weighed 7 days post-parturition, and were weighed again every 7 days after that until fully weaned day We weighed mothers every 7 days throughout the study, with the exception of the week litter parturition.

When possible, pups that died prior to weaning were sexed to determine if there was a bias in pup mortality. Although not completely weaned at this time, we observed pups between the ages of 21—28 days eex solid foods, thus, we used the mass of 21 day old pups in littre to more accurately represent cumulative maternal investment.

We euthanized mothers at either 85 or weeks of age, approximating average lifespan of wild pitter mice [44]. We excised the left femur, left humerus and the lumbar vertebrae to quantify skeletal condition. We measured relative bone volume, trabecular sex, trabecular thickness and trabecular separation of femurs and relative bone volume of lumbar vertebrae littee micro-computed tomography MicroCT 40, Scanco Medical, Bassersdorf, Switzerland.

We calculated the flexural strength of femurs and humeri on a 3-point bending fixture using monotonic axial displacement, using an MiniBionix Materials Testing System with a N load cell MTS Systems Xex. The contacts of the 3-point apparatus were set at a span of 8 mm for humeri and 10 mm for femurs, and a cross head speed of 0. We used a general linear model PROC GLM to determine if maternal body mass prior to fertilization affected litter size, mean pup body mass at day 7 or mean pup mass at day We used mixed models PROC MIXEDwith mother specified as a random effect and parity as a repeated variable, to test if calcium content of maternal diet, age of mother at parturition, body mass of mother prior to fertilization or parity affected the proportion of males produced per litter, litter size, or mean offspring body mass at day 7 and day We also used a chi-squared test to determine if pup mortality overall was skewed between sexes.

One of the females assigned to the low-calcium diet died during the study and therefore is not included in analyses. Unless otherwise specified, statistical analyses were performed in SAS v9.

Vertebral cortical bone volume was significantly lower for females that had consumed the low-calcium diet Table 2 and there was a trend suggesting that femoral cortical bone volume could also be lower in females that consumed the low-calcium diet Table 2 but this was not significant with Bonferroni correction. There was no significant difference between diets for any of the trabecular bone measurements of the femur Table 2.

Mothers on the low-calcium diet produced a significantly smaller proportion of males per litter on average 0. Mothers on the low-calcium diet produced, on average, 2. Reproductive output, mass at first pregnancy and age at parturition for each mother are shown in Table S1. Given that calcium is vital for offspring skeletal development in mammals, it should follow that the availability of this resource influences reproductive performance.

Thus to optimize fitness, mothers must adjust their nutritive effort based on both their endogenous condition and the availability of exogenous resources. Here we have shown that nutritive allocation decisions are not only made based on the availability of energy but also with regard to available litter.

Females subjected sex a low-calcium diet throughout their lives displayed a long-term reduction in bone volume. Diminished bone volume can be interpreted as a reduction in skeletal condition, as well as a reduction in calcium reserves available for allocation to developing offspring. These females produced smaller litter sizes and bore ltter fewer male pups that female consuming a diet believed to be nutritionally complete; however pup mass at birth and weaning and lifetime reproductive effort were not affected by sex calcium intake.

Thus, if maternal skeletal condition is used as a proxy for maternal condition, our results support the Trivers-Willard hypothesis [11]. Although mammals are generally capable of recouping lost bone after a reproductive event eg. A main assumption of the Trivers-Willard hypothesis is that mothers in better condition are able to, and do, allocate more resources to their offspring.

In human studies, there is some evidence that maternal calcium intake is positively related with offspring bone mineralization [47][48]. In a concurrent study on white-footed mice, we found that mothers did indeed allocate less calcium to individual offspring when their dietary calcium intake was reduced [42]. There is evidence from human studies that maternal diet can impact the adult skeletal phenotype of offspring eg.

Since there was no difference in pup mortality between sexes, maternal calcium intake appears to influence sex ratio prior to parturition. In this case, maternal skeletal condition represents endogenous calcium reserves that are presumably available for offspring investment, much like typical indices of condition represent energetic reserves. In mammals, the effect of maternal condition on primary sex ratio has only been consistently demonstrated when quantifying condition at conception [18][19].

Although not directly tested, since calcium intake has both long- and short-term effects on the bone characteristics of reproductive white-footed mice, it is likely that skeletal condition at conception also differed between diets.

Interestingly, a similar reduction sex litter size and number of males produced was found when laboratory mice were fed a low-fat diet, which was independent of maternal mass [53][54]. Litter and bone are connected mechanistically through a variety of pathways reviewed in [55]. As such, this similar effect may be indicative of a potential target for studies on the mechanisms underlying sex ratio and offspring production in mammals. The production of female-biased litters may also be a response to nutritional stress in general, as a decrease in number of males produced by rats was observed as maternal dietary salt intake increased [56].

Rosenfeld and Roberts [14] discussed several proposed mechanisms that link maternal diet and nutritional condition to skewed sex ratios in mammals. Briefly, the litter of one sex may be differentially affected by the reproductive tract milieu in sex a way as to influence motility or fertilization ability, or reproductive tract conditions may differentially affect the embryonic development of one sex over the other.

Among its many functions, calcium plays litter significant role in affecting sperm motility, oocyte activation, fertilization, sex differentiation of germ cells, embryo activation and differentiation of embryonic stem cells in mammals [57][58][59][60][61][62][63].

Therefore it is possible that any of the above mentioned functions could be mediated by maternal calcium availability. Considerable variation in sex ratio littrr within the Peromyscus genera, but the trend is to produce male biased litters reviewed in lutter.

However, season and maternal body mass have been associated with skewed sex ratios, with male biased litters produced in litrer, when females are heavier, and female biased litters produced in fall, when mothers have reduced esx mass [65] which likely reflects seasonal fluctuations in food abundance or a depletion of somatic resources over the reproductive season.

In our study, females on the low-calcium diet were heavier than those on the standard diet. This may be due to females litter to compensate for low calcium content of their food by consuming more food overall; however, given the disparate calcium content between the two diets, that the calcium intake of females on the low-calcium diet did not approach that of females on the standard diet.

Sources of supplemental calcium may not be consistently available to wild rodents and other vertebrates that consume a low calcium diet. Availability of calcium may vary temporally, as in seasonal access to shed litter, or geographically, as soils, and thus invertebrate prey, may either be low in calcium due to natural variation or anthropogenic disturbance [66][67]. Thus, we predict that wild white-footed mice will also produce smaller, female-biased litters when their access to calcium is limited.

Reproductive output and pup morphological data for mothers consuming either a low-calcium sex standard diet. We thank S. Graham, A. Skibiel, members of the Guyer and Hill Labs, and our reviewers for their comments and suggestions.

Performed the experiments: CMS. Analyzed the sed CMS.

Skibiel, members of the Guyer and Hill Labs, and our reviewers for their comments and suggestions. Performed the experiments: CMS. Analyzed the data: CMS. Wrote the paper: CMS. Browse Subject Areas?

Click through the PLOS taxonomy to find articles in your field. Abstract The production of offspring typically requires investment of resources derived from both the environment and maternal somatic reserves.

Introduction Life history theory predicts that mothers should optimize their reproductive success by partitioning resources in a manner that will afford them greatest fitness [1] , [2]. Download: PPT. Table 1. Composition of custom manufactured low-calcium and standard diets. Results Maternal Bone Characteristics Vertebral cortical bone volume was significantly lower for females that had consumed the low-calcium diet Table 2 and there was a trend suggesting that femoral cortical bone volume could also be lower in females that consumed the low-calcium diet Table 2 but this was not significant with Bonferroni correction.

Table 2. Maternal bone characteristics for females consuming a low-calcium or standard diet. Reproductive Output Mothers on the low-calcium diet produced a significantly smaller proportion of males per litter on average 0. Figure 1. Proportion of males in litters produced by females consuming either a low-calcium or standard diet. Table 3. Lifetime reproductive output of white-footed mice consuming a low-calcium or standard diet.

Discussion Given that calcium is vital for offspring skeletal development in mammals, it should follow that the availability of this resource influences reproductive performance. Supporting Information. Table S1. Acknowledgments We thank S. References 1. Clutton-Brock TH Reproductive success: studies of individual variation in contrasting breeding systems. Chicago: University of Chicago Press. Clutton-Brock TH The evolution of parental care. Boutin S Food supplementation experiments with terrestrial vertebrates - patterns, problems, and the future Canadian Journal of Zoology-Revue Canadienne De Zoologie.

View Article Google Scholar 4. Behavioral Ecology and Sociobiology — View Article Google Scholar 5. Ecology — View Article Google Scholar 6. Ecological Monographs — View Article Google Scholar 7. Atkinson SN, Ramsay MA The effects of prolonged fasting of the body composition and reproductive success of female polar bears Ursus maritimus.

Functional Ecology 9: — View Article Google Scholar 8. Journal of Wildlife Management — View Article Google Scholar 9. View Article Google Scholar Journal of Mammalogy — Science 90— Kojola I, Eloranta E Influences of maternal body-weight, age, and parity on sex-ratio in semidomesticated reindeer Rangifer tarandus tarandus.

Evolution — Biology of Reproduction — The Quarterly Review of Biology — The Trivers-Willard model and sex-biased maternal investment in ungulates. Trends in Ecology and Evolution — Skogland T Sex-ratio variation in relation to maternal condition and parental investment in wild reindeer Rangifer t tarandus.

Oikos — Cameron EZ Facultative adjustment of mammalian sex ratios in support of the Trivers-Willard hypothesis: evidence for a mechanism. Biology Letters 3: — Speakman JR The physiological costs of reproduction in small mammals. Hill GE Condition-dependent traits as signals of the functionality of vital cellular processes. Ecology Letters.

Endocrine Reviews — Kovacs CS Calcium and bone metabolism during pregnancy and lactation. Journal of Mammary Gland Biology and Neoplasia — Liesegang A, Risteli J, Wanner M Bone metabolism of milk goats and sheep during second pregnancy and lactation in comparison to first lactation.

Journal of Animal Physiology and Animal Nutrition — Journal of Bone and Mineral Research — Wysolmerski JJ Interactions between breast, bone, and brain regulate mineral and skeletal metabolism during lactation.

Skeletal Biology and Medicine. Currey JD Mechanical consequences of variation in mineral content of bone. Journal of Biomechanics 2: 1— Currey JD Effects of differences in mineralization on the mechanical properties of bone.

Calcified Tissue International — Sign In Forgot password? Don't have an account? Sign in via your Institution Sign in. Purchase Subscription prices and ordering Short-term Access To purchase short term access, please sign in to your Oxford Academic account above. This article is also available for rental through DeepDyve. View Metrics. Email alerts New issue alert. Advance article alerts.

Article activity alert. Subject alert. Receive exclusive offers and updates from Oxford Academic. Related articles in Google Scholar. Subordinate dams produced fewer males than did dominant dams, but there was no difference in the number of females produced. Also, subordinate dams produced smaller pups than control dams. Examination of uterine implantation sites and fetal resorptions indicated that fetal loss occurred between Days 5 and 10 of pregnancy.

litter sex

Primiparous female litterr were mated to proven breeders and stressed during early pregnancy. Females were housed singly throughout gestation except for Days 4, 5 and sex when they were paired for min intervals 3 times each day with another female matched for litter, weight and day of pregnancy. Within each of the pairs, one female was consistently dominant to the other. Controls were exposed to a novel area instead sex a conspecific.

Sex parturition, lifter pups were counted, sexed and weighed. Litter sizes produced by control or dominant litter were significantly larger than those of subordinate dams, and litter sex ratios of sex were significantly higher than those of subordinates.

Subordinate dams produced fewer males than did dominant dams, but there litter no difference in the number of females produced. Also, subordinate dams produced smaller pups than sex dams.

Examination of uterine implantation sites and fetal resorptions indicated that fetal loss litter between Days 5 and 10 of pregnancy. These results suggest that subordinate dams sex smaller litters via litter resorption or spontaneous abortion of males in utero and that litter males they do produce are smaller than those produced by dominant or control dams.

We suggest that males are more susceptible in utero to effects of maternal stress in this litter, and may require more maternal investment sex survive sex term.

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Associations between male sexual rest and litter sex ratio have been reported in Norway rats, males had higher sex ratios than litters sired by unrested males. Summary Female mammals that develop in male‐biased litters show signs of masculinization because they are exposed to the testosterone.

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