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.     

Sperm stratification and paternity success in red flour beetles

Abstract. When females are inseminated by multiple males, male paternity success (sperm precedence) is determined by the underlying processes of sperm storage and sperm utilization. Although informative for many questions, two-male sperm competition experiments may offer limited insight into natural mating scenarios when females are likely to mate with several males. In this study, genetic markers in Tribolium castaneum are used to trace paternity for multiple sires, and to determine whether displacement of stored sperm that occurs after a third mating equally affects both previous mates, or if fertilizations are disproportionately lost by the female's most recent mate. For 20 days after triple-matings, first males retain significantly higher paternity success (relative to first male paternity in double-matings) compared with second males. These results demonstrate that when females remate before sperm mixing occurs, sperm stratification results in differential loss of sperm from the most recent mate. This study provides insight into the mechanisms underlying sperm precedence in a promiscuous mating system, and suggests that T. castaneum females could limit paternity success of particular mates by remating with more highly preferred males.     

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.     

Susceptibility of last instar red flour beetles and confused flour beetles (Coleoptera: Tenebrionidae) to hydroprene.

Last instar larvae of the red flour beetle, Tribolium castaneum (Herbst), and the confused flour beetle, Tribolium confusum Jacquelin du Val, were either exposed for 8-144 h on concrete treated with 1.9 x 10(-3) mg(AI)/per cm2 hydroprene, or continually exposed on concrete treated with 9.8 x 10(-4) to 1.9 x 10(-3) mg[AI]/per cm2 hydroprene. In both tests, larvae were exposed and held at 27 or 32 degrees C and 40, 57, or 75% RH. When larvae were exposed with no food to hydroprene for different time intervals, then transferred to untreated concrete containing flour, consistent effects were produced only at 144 h. At this exposure interval, the percentage of beetles arrested in the larval stage after 3-4 wk was generally greater at 75% RH compared with 40 and 57% RH, but there were no differences between species or temperature. The percentages of dead adult red flour beetles and live adults with morphological deformities were also greatest at 75% RH, and defects were more prevalent in red flour beetles than in confused flour beetles. When larvae were continually exposed to different concentrations of hydroprene on concrete that contained flour, the percentage of arrested larvae, dead adults, and live adults of both species generally increased with concentration. There were more deleterious effects at 75% RH compared with either 40 or 57% RH, and effects were more pronounced in the red flour beetle compared with the confused flour beetle. In both experiments, temperature effects were variable and inconclusive. Results indicate that continual exposure of last instar red flour beetle and confused flour beetle to hydroprene can limit population development, but exposure intervals of >6 d may be required for maximum effectiveness.     

Polyandry and female control: the red flour beetle Tribolium castaneum as a case study

Females of many animal species are polyandrous, and there is evidence that they can control pre- and post-mating events. There has been a growing interest in consequences of polyandry for male and female reproductive success and offspring fitness, and its evolutionary significance. In several taxa, females exhibit mate choice both before and after mating and can influence the paternity of their offspring, enhancing offspring number and quality, but potentially countering male interests. Studying female mating biology and in particular post-copulatory female control mechanisms thus promises to yield insights into sexual selection and the potential of male-female coevolution. Here, we highlight the red flour beetle Tribolium castaneum (Herbst), a storage pest, as a model system to study polyandry, and review studies addressing the effects of polyandry on male sperm competitive ability and female control of post-mating events. These studies show that the outcome of sperm competition in the red flour beetle is influenced by both male and female traits. Furthermore, recent advances suggest that sexual conflict may have shaped reproductive traits in this species.     

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.     

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.     

High temperature intensifies negative density dependence of fitness in red flour beetles

Competition for food, space, or other depletable resources has strong impacts on the fitness of organisms and can lead to a pattern known as negative density dependence, where fitness decreases as population density increases. Yet, many resources that have strong impacts on fitness are nondepletable (e.g., moisture or temperature). How do these nondepletable resources interact with depletable resources to modify negative density dependence? We tested the hypothesis that negative density dependence is modulated by temperature in red flour beetles and tested the prediction that the strength of negative density dependence should decrease as temperature decreases. We measured the number of eggs laid, offspring development time, and the number of offspring that reached maturity at three temperatures and two food treatment combinations as we simultaneously manipulated adult population density. We demonstrated that low temperatures weaken negative density dependence in the number of eggs laid; this pattern was most evident when food was abundant. Density had no effect on development time, but low temperatures increased development time. The percent of eggs that emerged as adults decreased with both density and temperature and increased with food. Temperature, an abiotic driver, can thus modulate density-dependent processes in ectotherms. Therefore, models of population growth for ectotherms should incorporate the effects of temperature.     

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.     

Copulatory courtship and cryptic female choice in red flour beetles Tribolium castaneum

Males of many animal species engage in courtship behaviours during and after copulation that appear to be solely aimed at stimulating the female. It has been suggested that these behaviours have evolved by cryptic female choice, whereby females are thought to impose biases on male postmating paternity success. Males of the red flour beetle Tribolium castaneum rub the lateral edges of the females' elytra with their tarsi during copulation. We manipulated female perception of this behaviour by tarsal ablation in males, thus preventing males from reaching the edge of the female elytra with their manipulated legs, and by subsequently performing a series of double-mating experiments where the copulatory behaviour was quantified. We found a positive relationship between the intensity of the copulatory courtship behaviour and relative fertilization success among unmanipulated males. This pattern, however, was absent in manipulated males, where female perception of male behaviour differed from that actually performed. Thus, female perception of male copulatory courtship behaviour, rather than male behaviour per se, apparently governs the fate of sperm competing over fertilizations within the female, showing that copulatory courtship is under selection by cryptic female choice.     

Impact of food source on survival of red flour beetles and confused flour beetles (Coleoptera: Tenebrionidae) exposed to diatomaceous earth

A series of experiments was conducted to determine the effect of a flour food source on survival of red flour beetle, Tribolium castaneum (Herbst), and confused flour beetle, Tribolium confusum (DuVal), exposed to the labeled rate (0.5 mg/cm2) of Protect-It, a marine formulation of diatomaceous earth. Beetles were exposed at 27 degrees C, and 40, 57, and 75% RH in 62-cm2 petri dishes. When beetles were exposed for 1 or 2 d in dishes with the labeled rate (0.5 mg/cm2, or 31 mg per dish) of diatomaceous earth or in dishes containing flour at varying levels from 0 to 200 mg mixed with the labeled rate of diatomaceous earth, survival of both species increased as the amount of flour increased, and quickly plateaued at levels approaching 100%. In a second set of experiments, beetles were transferred to dishes containing flour at varying levels from 0 to 200 mg after they were exposed for 1 or 2 d in dishes with the labeled rate of diatomaceous earth alone. There were no significant differences in beetle survival among the levels of flour, however, survival in dishes with flour was usually greater than survival in dishes with diatomaceous earth alone. In a third test, beetles were exposed for 1, 2, and 3 d in dishes with either the labeled rate of diatomaceous earth alone (clean dishes), dishes with diatomaceous earth and empty straws, or dishes with diatomaceous earth and approximately 300 mg of flour packed in the straws. Survival was not significantly different between clean dishes or dishes with straws, but survival in dishes containing the straws with flour was usually 100%, regardless of exposure interval. In all experiments, confused flour beetles were less susceptible to diatomaceous earth than red flour beetles. In addition, survival was negatively related to exposure interval and positively related to relative humidity.     

Successful sons or superior daughters: sex-ratio variation in springbok

Mothers would often benefit from producing more offspring of one sex than the other. Although some species show an astonishing ability to skew their sex ratio adaptively, the trends found in many studies on vertebrates have proved inconsistent. Furthermore, evidence for a mechanism by which such a bias is achieved is equivocal at best. Here, we examine sex-ratio variation over 30 years, both at an individual and a population level, in the highly polygynous, size-dimorphic springbok (Antidorcas marsupialis). Many previous studies of similar species have shown that mothers in superior condition preferentially produce sons, whereas those in poorer condition produce more daughters. We found the opposite to be true in springbok, perhaps because daughters provide mothers in superior condition with a more rapid and secure fitness return. This theory was supported by the findings that earlier-conceived offspring tended to be female and that an increased proportion of daughters were produced with increasing rainfall (which was likely to reduce nutritional stress). We also show that selective reabsorption of embryos is unlikely to be the main mechanism by which deviations from an equal sex ratio are achieved. Hence, either differential implantation occurs or females are able to influence the sex of the sperm fertilizing an egg.     

Toxicity of diatomaceous earth to red flour beetles and confused flour beetles (Coleoptera: Tenebrionidae): effects of temperature and relative humidity

Red flour beetles, Tribolium castaneum (Herbst), and confused flour beetles, Tribolium confusum (DuVal), were exposed for 8-72 h to diatomaceous earth (Protect-It) at 22, 27, and 32 degrees C and 40, 57, and 75% RH (9 combinations). Insects were exposed to the diatomaceous earth at 0.5 mg/cm2 on filter paper inside plastic petri dishes. After exposure, beetles were held for 1 wk without food at the same conditions at which they were exposed. Mortality of both species after initial exposure was lowest at 22 degrees C but increased as temperature and exposure interval increased, and within each temperature decreased as humidity increased. With 2 exceptions, all confused flour beetles were still alive after they were exposed at 22 degrees C, 57 and 75% RH. Mortality of both species after they were held for 1 wk was greater than initial mortality for nearly all exposure intervals at each temperature-humidity combination, indicating delayed toxic effects from exposure to diatomaceous earth. For both species, the relationship between mortality and exposure interval for initial and 1-wk mortality was described by linear, nonlinear, quadratic, and sigmoidal regression. Mortality of confused flour beetles was lower than mortality of red flour beetles exposed for the same time intervals for 46.7% of the total comparisons at the various temperature-relative humidity combinations.     

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.     

Transgenerational effects of nutrition are different for sons and daughters

Food shortage is an important selective factor shaping animal life‐history trajectories. Yet, despite its role, many aspects of the interaction between parental and offspring food environments remain unclear. In this study, we measured developmental plasticity in response to food availability over two generations and tested the relative contribution of paternal and maternal food availability to the performance of offspring reared under matched and mismatched food environments. We applied a cross‐generational split‐brood design using the springtail Orchesella cincta, which is found in the litter layer of temperate forests. The results show adverse effects of food limitation on several life‐history traits and reproductive performance of both parental sexes. Food conditions of both parents contributed to the offspring phenotypic variation, providing evidence for transgenerational effects of diet. Parental diet influenced sons’ age at maturity and daughters’ weight at maturity. Specifically, being born to food‐restricted parents allowed offspring to alleviate the adverse effects of food limitation, without reducing their performance under well‐fed conditions. Thus, parents raised on a poor diet primed their offspring for a more efficient resource use. However, a mismatch between maternal and offspring food environments generated sex‐specific adverse effects: female offspring born to well‐fed mothers showed a decreased flexibility to deal with low‐food conditions. Notably, these maternal effects of food availability were not observed in the sons. Finally, we found that the relationship between age and size at maturity differed between males and females and showed that offspring life‐history strategies in O. cincta are primed differently by the parents.