Uteroplacental insufficiency and reducing litter size alters skeletal muscle mitochondrial biogenesis in a sex-specific manner in the adult rat

Uteroplacental insufficiency has been shown to impair insulin action and glucose homeostasis in adult offspring and may act in part via altered mitochondrial biogenesis and lipid balance in skeletal muscle. Bilateral uterine vessel ligation to induce uteroplacental insufficiency in offspring (Restricted) or sham surgery was performed on day 18 of gestation in rats. To match the litter size of Restricted offspring, a separate cohort of sham litters had litter size reduced to five at birth (Reduced Litter), which also restricted postnatal growth. Remaining litters from sham mothers were unaltered (Control). Offspring were studied at 6 mo of age. In males, both Restricted and Reduced Litter offspring had reduced gastrocnemius PPAR γ coactivator-1α (PGC-1 α) mRNA and protein, and mitochondrial transcription factor A (mtTFA) and cytochrome oxidase (COX) III mRNA (P < 0.05), whereas only Restricted had reduced skeletal muscle COX IV mRNA and protein and glycogen (P < 0.05), despite unaltered glucose tolerance, homeostasis model assessment (HOMA) and intramuscular triglycerides. In females, only gastrocnemius mtTFA mRNA was lower in Reduced Litter offspring (P < 0.05). Furthermore, glucose tolerance was not altered in any female offspring, although HOMA and intramuscular triglycerides increased in Restricted offspring (P < 0.05). It is concluded that restriction of growth due to uteroplacental insufficiency alters skeletal muscle mitochondrial biogenesis and metabolic characteristics, such as glycogen and lipid levels, in a sex-specific manner in the adult rat in the absence of impaired glucose tolerance. Furthermore, an adverse postnatal environment induced by reducing litter size also restricts growth and alters skeletal muscle mitochondrial biogenesis and metabolic characteristics in the adult rat.

Effect of pregnancy for females born small on later life metabolic disease risk

There is a strong inverse relationship between a females own birth weight and her subsequent risk for gestational diabetes with increased risk of developing diabetes later in life. We have shown that growth restricted females develop loss of glucose tolerance during late pregnancy with normal pancreatic function. 

Uteroplacental insufficiency leads to hypertension, but not glucose intolerance or impaired skeletal muscle mitochondrial biogenesis, in 12-month-old rats

Growth restriction impacts on offspring development and increases their risk of disease in adulthood which is exacerbated with "second hits." The aim of this study was to investigate if blood pressure, glucose tolerance, and skeletal muscle mitochondrial biogenesis were altered in 12-month-old male and female offspring with prenatal or postnatal growth restriction. Bilateral uterine vessel ligation induced uteroplacental insufficiency and growth restriction in offspring (Restricted). A sham surgery was also performed during pregnancy (Control) and some litters from sham mothers had their litter size reduced (Reduced litter), which restricted postnatal growth. Growth-restricted females only developed hypertension at 12 months, which was not observed in males. In Restricted females only homeostasis model assessment for insulin resistance was decreased, indicating enhanced hepatic insulin sensitivity, which was not observed in males. Plasma leptin was increased only in the Reduced males at 12 months compared to Control and Restricted males, which was not observed in females. Compared to Controls, leptin, ghrelin, and adiponectin were unaltered in the Restricted males and females, suggesting that at 12 months of age the reduction in body weight in the Restricted offspring is not a consequence of circulating adipokines. Skeletal muscle PGC-1α levels were unaltered in 12-month-old male and female rats, which indicate improvements in lean muscle mass by 12 months of age. In summary, sex strongly impacts the cardiometabolic effects of growth restriction in 12-month-old rats and it is females who are at particular risk of developing long-term hypertension following growth restriction.

The colour of paternity: extra-pair paternity in the wild Gouldian finch does not appear to be driven by genetic incompatibility between morphs

In socially monogamous species, individuals can use extra-pair paternity and offspring sex allocation as adaptive strategies to ameliorate costs of genetic incompatibility with their partner. Previous studies on domesticated Gouldian finches (Erythrura gouldiae) demonstrated a genetic incompatibility between head colour morphs, the effects of which are more severe in female offspring. Domesticated females use differential sex allocation, and extra-pair paternity with males of compatible head colour, to reduce fitness costs associated with incompatibility in mixed-morph pairings. However, laboratory studies are an oversimplification of the complex ecological factors experienced in the wild, and may only reflect the biology of a domesticated species. This study aimed to examine the patterns of parentage and sex-ratio bias with respect to colour pairing combinations in a wild population of the Gouldian finch. We utilized a novel PCR assay that allowed us to genotype the morph of offspring before the morph phenotype develops, and to explore bias in morph paternity and selection at the nest. Contrary to previous findings in the laboratory, we found no effect of pairing combinations on patterns of extra-pair paternity, offspring sex ratio, or selection on morphs in nestlings. In the wild, the effect of morph incompatibility is likely much smaller, or absent, than was observed in the domesticated birds. Furthermore, the previously studied domesticated population is genetically differentiated from the wild population, consistent with the effects of domestication. It is possible that the domestication process fostered the emergence (or enhancement) of incompatibility between colour morphs previously demonstrated in the laboratory.

Male and female effects on fertilization success and offspring viability in the Peron's tree frog, Litoria peronii

There is increasing theoretical and empirical evidence that genetic compatibility among partners is an important determinant of fertilization success and offspring viability. In amphibians, females often actively choose partners from among a variety of males and polyandry is common. Genetic compatibility among partners may therefore be an important determinant of fertilization success and offspring viability in some amphibians. Amphibians also show some of the highest levels of genetic differentiation among neighbouring populations known in vertebrates, and as such, populations may have evolved different co-adapted gene complexes. This means that offspring from among-population crosses may have reduced fitness. It is therefore essential to understand to what extent crossings between and within populations may interfere with successful fertilization and offspring viability. Here, we test whether crossing individuals within and between two different populations of the Australian Peron's tree frog (Litoria peronii) using artificial fertilizations affect fertilization success and offspring viability. Fertilization success per se is strongly influenced by male identity, which is likely to depend at least to some extent on the experimental procedure (e.g. resulting in variation in sperm number per ejaculate), whereas there was no fertilization effect of female identity. More importantly, male and female identity, independently of each other, explained significant variation in offspring viability, whereas no such effect could be linked to population of origin. Thus, our experiments suggest that crossing populations may not always be the most significant factor affecting fertilization success or offspring viability, but may be more influenced by the genetic quality or the genetic compatibility of partners.

Different male vs. female breeding periodicity helps mitigate offspring sex ratio skews in sea turtles

 The implications of climate change for global biodiversity may be profound with those species with little capacity for adaptation being thought to be particularly vulnerable to warming. A classic case of groups for concern are those animals exhibiting temperature-dependent sex-determination (TSD), such as sea turtles, where climate warming may produce single sex populations and hence extinction. We show that, globally, female biased hatchling sex ratios dominate sea turtle populations (exceeding 3:1 in >50% records), which, at-a-glance, reiterates concerns for extinction. However, we also demonstrate that more frequent breeding by males, empirically shown by satellite tracking 23 individuals and supported by a generalized bio-energetic life history model, generates more balanced operational sex ratios (OSRs). Hence, concerns of increasingly skewed hatchling sex ratios and reduced population viability are less acute than previously thought for sea turtles. In fact, in some scenarios skewed hatchling sex ratios in groups with TSD may be adaptive to ensure optimum OSRs.

Song and female choice for extrapair copulations in the sedge warbler, Acrocephalus schoenobaenus

Although 90% of passerine birds live in socially monogamous pair bonds, molecular studies have revealed that genetic polygamy occurs in 86% of surveyed passerines, because individuals engage in copulations outside the pair bond (extrapair copulations; EPCs). Most explanations for the occurrence of EPCs involve female gaining indirect benefits from the extrapair male. The sedge warbler is a socially monogamous species in which some offspring result from EPCs (8% in this study). Complex song is a sexually selected male trait used by females which select mates based on a variety of male qualities. We used microsatellite DNA profiling to detect extrapair young and assign paternity. ‘Good genes’ theory predicts that females should engage in EPCs with males of higher quality than their social mate, with resulting fitness benefits. Extrapair males had smaller song repertoires and smaller territories than the social mate. This apparent preference for small-repertoire males as extrapair mates conflicts with the predictions from previous studies of this species. Sudden cessation of song after pairing may mean that song cues are unavailable for later extrapair matings and females may switch to other cues. Such behaviour may lead to different patterns of female choice during social and extrapair mating in the sedge warbler. We conclude that multiple reasons underlie patterns of female choice in this species.

Sperm competition and offspring viability at hybridization in Australian tree frogs, Litoria peronii and L. tyleri

Hybridization between closely related species often leads to reduced viability or fertility of offspring. Complete failure of hybrid offspring (post-zygotic hybrid incompatibilities) may have an important role in maintaining the integrity of reproductive barriers between closely related species. We show elsewhere that in Peron's tree frog, Litoria peronii, males more closely related to a female sire more offspring in sperm competition with a less related rival male. Observations of rare 'phenotypic intermediate' males between L. peronii and the closely related L. tyleri made us suggest that these relatedness effects on siring success may be because of selection arising from risks of costly hybridization between the two species. Here, we test this hypothesis in an extensive sperm competition experiment, which shows that there is no effect of species identity on probability of fertilization in sperm competition trials controlling for sperm concentration and sperm viability. Instead, there was a close agreement between a male's siring success in isolation with a female and his siring success with the same female in competition with a rival male regardless of species identity. Offspring viability and survival, however, were strongly influenced by species identity. Over a 14-day period, hybrid offspring suffered increasing mortality and developed more malformations and an obvious inability to swim and right themselves, leading to compromised probability of survival. Thus, hybridization in these sympatric tree frogs does not compromise fertilization but has a strong impact on offspring viability and opportunity for reinforcement selection on mate choice for conspecific partners.

Breeding ecology and bias in offspring sex ratio in little grassbirds (Megalurus gramineus)

Little grassbirds (Megalurus gramineus) are small, sexually monomorphic passerines that live in reed beds, lignum swamps and salt marshes in southern Australia. The breeding biology and patterns of sex allocation of the little grassbird were investigated over a single breeding season. Our observations of this species in the Edithvale Wetland Reserve revealed a highly male-biased population sex ratio, with some breeding territories containing several additional males. Nevertheless, there was little compelling evidence that little grassbirds breed cooperatively. The growth rates of male and female nestlings were similar and, as predicted by theory, there was no overall primary sex ratio bias. However, the primary sex ratio was female-biased early in the breeding season and became increasingly male-biased later in the breeding season.

Does female nuptial coloration reflect egg carotenoids and clutch quality in the Two-Spotted Goby (Gobiusculus flavescens, Gobiidae)?

Summary

1 - Carotenoid-based ornamentation has often been suggested to signal mate quality, and species with such ornaments have frequently been used in studies of sexual selection.

2 - Female Gobiusculus flavescens (Two-Spotted Goby) develop colourful orange bellies during the breeding season. Belly coloration varies among mature females, and previous work has shown that nest-holding males prefer females with more colourful bellies. Because males invest heavily in offspring during incubation, the evolution of this preference can be explained if colourful females provide males with eggs of higher quality.

3 - We tested this hypothesis by allowing males to spawn with ‘colourful’ and ‘drab’ females and comparing parameters including egg carotenoid concentration, clutch size, hatchability and larval viability between groups. We also investigated relationships between egg carotenoid concentration and clutch quality parameters.

4 - Eggs from colourful females had significantly higher concentrations of total carotenoids than drab females, and photographically quantified belly coloration was a good predictor of egg carotenoid concentration.

5 - Colourful females produced slightly larger clutches, but female belly coloration was not related to any measure of clutch quality. In addition, there were no significant relationships between egg carotenoids and clutch quality. Females with high levels of egg carotenoids spawned slightly earlier, however, possibly because they were more ready to spawn or because of male mate choice.

6 - Our results call into question the generality of a causal link between egg carotenoids and offspring quality.

Maternal stress to partner quality is linked to adaptive offspring sex ratio adjustment

Female birds have been shown to have a remarkable degree of control over the sex ratio of the offspring they produce. However, it remains poorly understood how these skews are achieved. Female condition, and consequent variation in circulating hormones, provides a plausible mechanistic link between offspring sex biases and the environmental and social stresses commonly invoked to explain adaptive sex allocation, such as diet, territory quality, and body condition. However, although experimental studies have shown that female perception of male phenotype alone can lead to sex ratio biases, it is unknown how partner quality influences female physiological state. Using a controlled within-female experimental design where female Gouldian finches (Erythrura gouldiae) bred with both high- and low-quality males, we found that partner quality directly affects female hormonal status and subsequent fitness. When constrained to breeding with low-quality males, females had highly elevated stress responses (corticosterone levels) and produced adaptive male-biased sex ratios, whereas when they bred with high-quality males, females had low corticosterone levels and produced an equal offspring sex ratio. There was no effect of other maternal hormones (e.g., testosterone) or body condition on offspring sex ratios. Female physiological condition during egg production, and variation in circulating hormones in particular, may provide a general mechanistic route for strategic sex allocation in birds.

Mothers adjust offspring sex to match the quality of the rearing environment

Theory predicts that mothers should adjust offspring sex ratios when the expected fitness gains or rearing costs differ between sons and daughters. Recent empirical work has linked biased offspring sex ratios to environmental quality via changes in relative maternal condition. It is unclear, however, whether females can manipulate offspring sex ratios in response to environmental quality alone (i.e. independent of maternal condition). We used a balanced within-female experimental design (i.e. females bred on both low- and high-quality diets) to show that female parrot finches (Erythrura trichroa) manipulate primary offspring sex ratios to the quality of the rearing environment, and not to their own body condition and health. Individual females produced an unbiased sex ratio on high-quality diets, but over-produced sons in poor dietary conditions, even though they maintained similar condition between diet treatments. Despite the lack of sexual size dimorphism, such sex ratio adjustment is in line with predictions from sex allocation theory because nutritionally stressed foster sons were healthier, grew faster and were more likely to survive than daughters. These findings suggest that mothers may adaptively adjust offspring sex ratios to optimally match their offspring to the expected quality of the rearing environment.

Detecting female precise natal philopatry in green turtles using assignment methods

It is well established that sea turtles return to natal rookeries to mate and lay their eggs, and that individual females are faithful to particular nesting sites within the rookery. Less certain is whether females are precisely returning to their natal beach. Attempts to demonstrate such precise natal philopatry with genetic data have had mixed success. Here we focused on the green turtles of three nesting sites in the Ascension Island rookery, separated by 5–15 km. Our approach differed from previous work in two key areas. First, we used male microsatellite data (five loci) reconstructed from samples collected from their offspring (N = 17) in addition to data for samples taken directly from females (N = 139). Second, we employed assignment methods in addition to the more traditional F-statistics. No significant genetic structure could be demonstrated with FST. However, when average assignment probabilities of females were examined, those for nesting populations in which they were sampled were indeed significantly higher than their probabilities for other populations (Mann–Whitney U-test: P < 0.001). Further evidence was provided by a significant result for the mAIC test (P < 0.001), supporting greater natal philopatry for females compared with males. The results suggest that female natal site fidelity was not sufficient for significant genetic differentiation among the nesting populations within the rookery, but detectable with assignment tests.