Drivers of sex ratio bias in the eastern bongo: lower inbreeding increases the probability of being born male.

Parent sex ratio allocation has consequences for individual fitness, population dynamics, and conservation. Theory predicts that parents should adjust offspring sex ratio when the fitness returns of producing male or female offspring varies. Previous studies have assumed that only mothers are capable of biasing offspring sex ratios, but have neglected fathers, given the expectation of an equal proportion of X- and Y-chromosome-bearing (CBS) sperm in ejaculates due to sex chromosome segregation at meiosis. This assumption has been recently refuted and both paternal fertility and paternal genetic quality have been shown to bias sex ratios. Here, we simultaneously test the relative contribution of paternal, maternal, and individual genetic quality, as measured by inbreeding, on the probability of being born a son or a daughter, using pedigree and lifelong offspring sex ratio data for the eastern bongo ( Tragelaphus eurycerus isaaci). Our models showed first, that surprisingly, as individual inbreeding decreases the probability of being born male increases, second, that paternal genetic effects on sex ratio were stronger than maternal genetic effects (which were absent). Furthermore, paternal effects were opposite in sign to those predicted; father inbreeding increases the probability of having sons. Previous paternal effects have been interpreted as adaptive due to sex-specific inbreeding depression for reproductive traits. We argue that in the eastern bongo, the opposite sign of the paternal effect on sex ratios results from a reversed sex-specific inbreeding depression pattern (present for female but not male reproductive traits). We anticipate that this research will help stimulate research on evolutionary constraints to sex ratios. Finally, the results open a new avenue of research to predict sex ratio allocation in an applied conservation context. Future models of sex ratio allocation should also include the predicted inbreeding level of the offspring and paternal inbreeding levels.

The diversity of population responses to environmental change.

The current extinction and climate change crises pressure us to predict population dynamics with ever-greater accuracy. Although predictions rest on the well-advanced theory of age-structured populations, two key issues remain poorly explored. Specifically, how the age-dependency in demographic rates and the year-to-year interactions between survival and fecundity affect stochastic population growth rates. We use inference, simulations and mathematical derivations to explore how environmental perturbations determine population growth rates for populations with different age-specific demographic rates and when ages are reduced to stages. We find that stage- vs. age-based models can produce markedly divergent stochastic population growth rates. The differences are most pronounced when there are survival-fecundity-trade-offs, which reduce the variance in the population growth rate. Finally, the expected value and variance of the stochastic growth rates of populations with different age-specific demographic rates can diverge to the extent that, while some populations may thrive, others will inevitably go extinct.

A father effect explains sex-ratio bias.

Sex ratio allocation has important fitness consequences, and theory predicts that parents should adjust offspring sex ratio in cases where the fitness returns of producing male and female offspring vary. The ability of fathers to bias offspring sex ratios has traditionally been dismissed given the expectation of an equal proportion of X- and Y-chromosome-bearing sperm (CBS) in ejaculates due to segregation of sex chromosomes at meiosis. This expectation has been recently refuted. Here we used Peromyscus leucopus to demonstrate that sex ratio is explained by an exclusive effect of the father, and suggest a likely mechanism by which male-driven sex-ratio bias is attained. We identified a male sperm morphological marker that is associated with the mechanism leading to sex ratio bias; differences among males in the sperm nucleus area (a proxy for the sex chromosome that the sperm contains) explain 22% variation in litter sex ratio. We further show the role played by the sperm nucleus area as a mediator in the relationship between individual genetic variation and sex-ratio bias. Fathers with high levels of genetic variation had ejaculates with a higher proportion of sperm with small nuclei area. This, in turn, led to siring a higher proportion of sons (25% increase in sons per 0.1 decrease in the inbreeding coefficient). Our results reveal a plausible mechanism underlying unexplored male-driven sex-ratio biases. We also discuss why this pattern of paternal bias can be adaptive. This research puts to rest the idea that father contribution to sex ratio variation should be disregarded in vertebrates, and will stimulate research on evolutionary constraints to sex ratios-for example, whether fathers and mothers have divergent, coinciding, or neutral sex allocation interests. Finally, these results offer a potential explanation for those intriguing cases in which there are sex ratio biases, such as in humans.

From physiology to space use: energy reserves and androgenization explain home-range size variation in a woodland rodent.

This study tested the relationships between both individual-level and predation-risk factors and the size of two home-range regions (HRR), defined as areas of different intensities of use. We have expanded on previous home-range studies by testing the effects of two previously ignored individual-level factors: androgenization and energy reserves (body fat). Location data were collected for wild individuals of Apodemus sylvaticus using the novel method of implanted PIT tags and mobile recording stations. A total of 68 home ranges were estimated using kernel density estimation. Home ranges were split into two regions (HRR): the 'core', representing the most intensively used areas, and 'periphery' regions. Body mass, body fat, sex, anogenital distance (AGD) (a proxy for androgenization) and the proportion of HRR, covered by antipredatory features (shrubs and fallen trees), were tested for their relationship with the size of core and periphery HRRs. Models were constructed for each HRR for three seasons: nonbreeding season (NBS), early and late breeding seasons (LBSs), to account for seasonal variation in behaviour associated with changes in food abundance and reproductive cycles. Body fat had a negative relationship with periphery size and an interaction with sex on core size in the early breeding season (EBS). Body mass also had a significant interaction with sex on core size in the EBS. Androgenization has a strong effect on home range size in both sexes: AGD had a positive relationship with both HRRs for males in the LBS and females in the NBS. Males had larger peripheries than females in both early and LBSs. Habitat features that reduce predation risk explain HRR size throughout the breeding period. This study emphasizes the importance of embracing natural complexity to gain insight into the drivers of space use behaviour; the consideration of individual and ecological factors, the recognition of the species-specific selective pressures that seasonal change presents for each sex and the identification of biologically meaningful home range areas will help advance the field.

Effects of genetic captive-breeding protocols on sperm quality and fertility in the white-footed mouse.

Mice (Peromyscus leucopus noveboracensis) from a captive-breeding program were used to test the effects of three genetic breeding protocols (minimizing mean kinship [MK], random breeding, and selection for docility [DOC]) and inbreeding levels on sperm traits and fertility. Earlier, in generation 8, one DOC replicate went extinct because of poor reproductive success. By generation 10, spermatozoa from DOC mice had more acrosome and midpiece abnormalities, which were shown to be strong determinants of fertility, as well as lower sperm production and resistance to osmotic stress. In addition, determinants of fertility, including male and female components, were assessed in a comprehensive manner. Results showed that the probability (P) of siring litters is determined by sperm number, sperm viability, and midpiece and acrosome abnormalities; that the P of siring one versus two litters is determined by tail abnormalities; and that the total number of offspring is influenced by female size and proportion of normal sperm, showing the relative importance of different sperm traits on fertility. On average, males with 20% normal sperm sired one pup per litter, and males with 70% normal sperm sired eight pups per litter. Interestingly, the proportion of normal sperm was affected by docility but not by relatively low inbreeding. However, inbreeding depression in sperm motility was detected. In the MK group, inbreeding depression not only affected sperm motility but also fertility: An increase in the coefficient of inbreeding (f) of 0.03 reduced sperm motility by 30% and translated into an offspring reduction of three pups in second litters. A genetic load of 48 fecundity equivalents was calculated.

Heterozygosity-fitness correlations and associative overdominance: new detection method and proof of principle in the Iberian wild boar.

Heterozygosity-fitness correlations (HFC) may result from a genome-wide process--inbreeding--or local effects within the genome. The majority of empirical studies reporting HFCs have attributed correlations to inbreeding depression. However, HFCs are unlikely to be caused by inbreeding depression because heterozygosity measured at a small number of neutral markers is unlikely to accurately capture a genome-wide pattern. Testing the strengths of localized effects caused by associative overdominance has proven challenging. In their current paper, Amos and Acevedo-Whitehouse present a novel test for local HFCs. Using stochastic simulations, they determine the conditions under which single-locus HFCs arise, before testing the strength of the correlation between the neutral marker and a linked gene under selection in their simulations. They used insights gained from simulation to statistically investigate the likely cause of correlations between heterozygosity and disease status using data on bovine tuberculosis infections in a wild boar population. They discover that a single microsatellite marker is an excellent predictor of tuberculosis progression in infected individuals. The results are relevant for wild boar management but, more generally, they demonstrate how single-locus HFCs could be used to identify coding loci under selection in free-living populations.

Sperm traits and male fertility in natural populations.

Male fertility has seldom been studied in natural populations because it has been assumed that strong selection would result in uniformly high values among males, and therefore mating success has been equated with fertilisation success. In contrast, male fertility has received much attention in studies of domestic livestock, where economic benefits rely on improving productivity, and in human infertility studies, where the efficiency of treatments depends on understanding which ejaculate traits explain reproductive failures and predict success at assisted conception. Despite years of efforts, no conclusive results have been obtained, probably because such studies have focused on opposite extremes of the range with little variation: domestic livestock have often been subject to strong artificial selection for high fertility, and human patients requiring treatment have compromised fertility. Recent findings from natural populations of red deer have shown that males differ markedly in their fertility, and have revealed the degree of variation found in different semen traits, both between and within males. Fertility trials have shown that male fertility is determined mainly by sperm swimming speed and the proportion of normal sperm, when sperm numbers are kept constant. Sperm design exerts a strong influence on sperm swimming speed, with faster swimming sperm having elongated heads, shorter midpieces and a longer principal plus terminal pieces in relation to total flagellum length. Thus, the large inter-male variation in sperm design found among natural populations underlies differences in sperm swimming speed which, in turn, determine differences in male fertility rates. Secondary sexual characters are honest indicators of male fertility, so males with large and elaborated antlers have larger testes and faster swimming sperm. Testosterone does not seem to mediate the relationship between antler size and semen quality, since it is associated with sperm production, but not with sperm quality or antler size. Finally, more fertile males produce a greater proportion of sons, who will inherit the semen traits which will enhance their fertility.

Male fertility and sex ratio at birth in red deer.

Efforts to test sex ratio theory have focused mostly on females. However, when males possess traits that could enhance the reproductive success of sons, males would also benefit from the manipulation of the offspring sex ratio. We tested the prediction that more-fertile red deer males produce more sons. Our findings reveal that male fertility is positively related to the proportion of male offspring. We also show that there is a positive correlation between the percentage of morphologically normal spermatozoa (a main determinant of male fertility) and the proportion of male offspring. Thus, males may contribute significantly to biases in sex ratio at birth among mammals, creating the potential for conflicts of interest between males and females.

Sperm design and sperm function.

Spermatozoa vary enormously in their form and dimensions, both between and within species, yet how this variation translates into fertilizing efficiency is not known. Sperm swimming velocity is a key determinant of male fertilization success, but previous efforts to identity which sperm phenotypic traits are associated with swimming velocity have been unsuccessful. Here, we examine the relationship between the size of several sperm components and sperm swimming velocity in natural populations of red deer (Cervus elaphus hispanicus) where selective pressures to enhance male reproductive success are expected to be strong. Our results show that there is little within-male and considerable between-male variation in sperm dimensions. Spermatozoa with longer midpieces swim more slowly, a finding which does not support the hypothesis that the size of the midpiece determines the amount of energy which is translated into swimming speed. In contrast, spermatozoa with elongated heads, and those in which the relative length of the rest of the flagellum is longer, swim faster. Thus, the hydrodynamic shape of the head and the forces generated by the relative size of the rest of the flagellum seem to be the key determinants of sperm swimming velocity.

Antlers honestly advertise sperm production and quality.

Evolutionary theory proposes that exaggerated male traits have evolved via sexual selection, either through female mate choice or male-male competition. While female preferences for ornamented males have been amply demonstrated in other taxa, among mammals sexual characters are commonly regarded as weapons whose main function is to enhance male competitiveness in agonistic encounters. One particularly controversial hypothesis to explain the function of male sexual characters proposes that they advertise male fertility. We test this hypothesis in red deer (Cervus elaphus), a species where sexual characters (antlers) reach an extreme degree of elaboration. We find that a global measure of relative antler size and complexity is associated with relative testes size and sperm velocity. Our results exclude the possibility that condition dependence, age or time of culling, drive these associations. Red deer antlers could signal male fertility to females, the ability to avoid sperm depletion throughout the reproductive season and/or the competitive ability of ejaculates. By contrast, male antlers could also signal to other males not only their competitive ability at the behavioural level (fighting ability) but also at the physiological level (sperm competition).

Male fertility in natural populations of red deer is determined by sperm velocity and the proportion of normal spermatozoa.

Male reproductive success is determined by the ability of males to gain sexual access to females and by their ability to fertilize ova. Among polygynous mammals, males differ markedly in their reproductive success, and a great deal of effort has been made to understand how selective forces have shaped traits that enhance male competitiveness both before and after copulation (i.e., sperm competition). However, the possibility that males also may differ in their fertility has been ignored under the assumption that male infertility is rare in natural populations because selection against it is likely to be strong. In the present study, we examined which semen traits correlate with male fertility in natural populations of Iberian red deer (Cervus elaphus hispanicus). We found no trade-offs between semen traits. Our analyses revealed strong associations between sperm production and sperm swimming velocity, sperm motility and proportion of morphologically normal spermatozoa, and sperm viability and acrosome integrity. These last two variables had the lowest coefficients of variation, suggesting that these traits have stabilized at high values and are unlikely to be related to fitness. In a fertility trial, our results show a large degree of variation in male fertility, and differences in fertility were determined mainly by sperm swimming velocity and by the proportion of morphologically normal sperm. We conclude that male fertility varies substantially in natural populations of Iberian red deer and that, when sperm numbers are equal, it is determined mainly by sperm swimming velocity and sperm morphology.