Maternal Dppa2 and Dppa4 are dispensable for zygotic genome activation but important for offspring survival

ABSTRACT Zygotic genome activation (ZGA) represents the initiation of transcription following fertilisation. Despite its importance, we know little of the molecular events that initiate mammalian ZGA in vivo. Recent in vitro studies in mouse embryonic stem cells have revealed developmental pluripotency associated 2 and 4 (Dppa2/4) as key regulators of ZGA-associated transcription. However, their roles in initiating ZGA in vivo remain unexplored. We reveal that Dppa2/4 proteins are present in the nucleus at all stages of preimplantation development and associate with mitotic chromatin. We generated conditional single and double maternal knockout mouse models to deplete maternal stores of Dppa2/4. Importantly, Dppa2/4 maternal knockout mice were fertile when mated with wild-type males. Immunofluorescence and transcriptome analyses of two-cell embryos revealed that, although ZGA took place, there were subtle defects in embryos that lacked maternal Dppa2/4. Strikingly, heterozygous offspring that inherited the null allele maternally had higher preweaning lethality than those that inherited the null allele paternally. Together, our results show that although Dppa2/4 are dispensable for ZGA transcription, maternal stores have an important role in offspring survival, potentially via epigenetic priming of developmental genes.

Tadpole-transporting frogs use stagnant water odor to find pools in the rainforest

Breeding sites are often a limited and ephemeral resource for rainforest frogs. This resource limitation has driven the evolution of diverse reproductive strategies that increase offspring survival. For example, poison frogs shuttle their tadpoles from terrestrial clutches to aquatic rearing sites, using various cues to assess pool suitability. Yet, how frogs find new pools is unknown. We tested the role of odor cues in the process of finding tadpole deposition sites by the poison frog Allobates femoralis. We created 60 artificial pools grouped into three conditions: stagnant water, tadpole water, and clean water control. Fifteen pools were discovered within six days, with more tadpoles and more frogs directly observed at pools with stagnant odor cues. Our findings suggest that frogs use odor cues associated with stagnant water for the initial discovery of new breeding pools. These cues may be good indicators of pool stability and increased likelihood of tadpole survival.

Longitudinal evidence that older parents produce offspring with longer telomeres in a wild social bird

As telomere length (TL) often predicts survival and lifespan, there is considerable interest in the origins of inter-individual variation in TL. Cross-generational effects of parental age on offspring TL are thought to be a key source of variation, but the rarity of longitudinal studies that examine the telomeres of successive offspring born throughout the lives of parents leaves such effects poorly understood. Here, we exploit TL measures of successive offspring produced throughout the long breeding tenures of parents in wild white-browed sparrow weaver ( Plocepasser mahali ) societies, to isolate the effects of within-parent changes in age on offspring TLs. Our analyses reveal the first evidence to date of a positive within-parent effect of advancing age on offspring TL: as individual parents age, they produce offspring with longer telomeres (a modest effect that persists into offspring adulthood). We consider the potential for pre- and post-natal mechanisms to explain our findings. As telomere attrition predicts offspring survival to adulthood in this species, this positive parental age effect could impact parent and offspring fitness if it arose via differential telomere attrition during offspring development. Our findings support the view that cross-generational effects of parental age can be a source of inter-individual variation in TL.

The Costs and Benefits of Two Secondary Symbionts in a Whitefly Host Shape Their Differential Prevalence in the Field

Insects commonly harbor maternally inherited intracellular symbionts in nature, and the microbial partners often exert influence on host reproduction and fitness to promote their prevalence. Here, we investigated composition of symbionts and their biological effects in the invasive Bemisia tabaci MED species of a whitefly complex. Our field surveys revealed that populations of the MED whitefly, in addition to the primary symbiont Portiera, mainly contain two secondary symbionts Hamiltonella, which is nearly fixed in the host populations, and Cardinium with infection frequencies ranging from 0 to 86%. We isolated and established Cardinium-positive and Cardinium-free whitefly lines with a similar nuclear genetic background from a field population, and compared performance of the two whitefly lines. The infection of Cardinium incurred significant fitness costs on the MED whitefly, including reduction of fecundity and egg viability as well as delay in development. We then selectively removed Hamiltonella from the Cardinium-free whitefly line and compared performance of two whitefly lines, one harboring both Portiera and Hamiltonella and the other harboring only Portiera. While depletion of Hamiltonella had little or only marginal effects on the fecundity, developmental rate, and offspring survival, the Hamiltonella-free whitefly line produced very few female offspring, often reducing the progeny female ratio from about 50% to less than 1%. Our findings indicate that the varying costs and benefits of the association between these two symbionts and the MED whitefly may play an important role in shaping their differential prevalence in the field.

The Number of Offspring Weaned from Ewe Lambs Is Affected Differently by Liveweight and Age at Breeding

In this paper, we tested the hypothesis that ewe lambs that are heavier and older at breeding will wean more offspring, due to increased reproductive rate and offspring survival and lower maternal mortality. To test this hypothesis, we analyzed data from more than 11,500 maternal composite ewe lambs collected over eight years. The ewe lambs had full pedigree records including birth type, age and liveweight at breeding plus records of the birthweight and survival of their offspring and the dam. The average liveweight and age at breeding was 40.2 kg and 228 days. The reproductive rate and weaning rate responses to liveweight at breeding were curvilinear (p < 0.001), and if ewe lambs achieved 45 kg by the start of breeding, their reproductive rate and weaning rate were within 5% of their maximum. By contrast, the effects of age at breeding on weaning rate was linear and increased by 0.4% per day, despite a quadratic (p < 0.01) effect of age at breeding on reproductive rate which increased only marginally when ewe lambs were older than 8 months at breeding. Increasing liveweight (p < 0.05) or age (p < 0.001) at breeding increased survival of their offspring, however an extra 10 kg of liveweight or 30 days of age at breeding increased offspring survival by less than 5%. Both liveweight (p < 0.001) and age (p < 0.01) at breeding also influenced survival of the ewe lamb dam but survival rates exceeded 95% across the range in liveweights from 30 to 55 kg and ages from 6 to 9 months. This understanding of the trade-off between age and liveweight at breeding will assist farmers to optimize the management of their ewe lambs, given the earlier they can be bred successfully the easier they can be integrated with the breeding of the adult ewe flock the following year.

Number and Size of Offspring

Offspring number and size are two of the most variable life-history traits. Among species, much of this variability can be attributed to genetic, developmental, physiological, or structural constraints. Some trait combinations are not possible because of differences associated with a species’ evolutionary history. Substantial variation in propagule number and size can exist among populations of the same species, generating questions concerning the adaptive significance of this variability. The most influential models are those attributed to Lack on clutch size and to Smith and Fretwell on offspring size. Fundamental to both sets of models is a trade-off between offspring number and parental investment per offspring. When offspring survival or fitness continuously varies with offspring size, the fitness of the parent depends on both offspring size and the number of offspring of that size that the parent can produce. If offspring survival is independent of offspring size, parental fitness is maximized when individuals maximize the production of minimally sized propagules.

Advanced Paternal Age With Risk of Lifespan in Male Offspring Using Chinese Genealogical Data

Background Advanced paternal age has been associated with a variety of adverse reproductive outcomes. However, the effects of paternal age on offspring lifespan are still controversial. Result Here, we studied the correlation between parental reproductive age and offspring lifespan using a Chinese specific genealogy data. We chose a “Ding” genealogy data across 130 years during the Qing Dynasty (1726-1855). The present study showed that fathers aged more than 35 years were more likely to have male offspring with lower lifetime compared with fathers aged 20-35 years. The significant negative correlation between paternal age and male offspring lifespan existed after adjusted for maternal age. We proposed a new evidence that advanced paternal age is a risk for male offspring survival.

Maternal Dppa2 and Dppa4 are dispensable for zygotic genome activation but important for offspring survival

Zygotic Genome Activation (ZGA) represents the initiation of transcription following fertilisation. Despite its importance in shifting developmental control from primarily maternal stores in the oocyte to the embryo proper, we know little of the molecular events that initiate ZGA in vivo. Recent in vitro studies in mouse embryonic stem cells (ESCs) have revealed Developmental Pluripotency Associated 2 and 4 (Dppa2/4) as key regulators of ZGA-associated transcription. However, their roles in initiating ZGA in vivo remain unexplored. We reveal Dppa2/4 proteins are present in the nucleus at all stages of preimplantation development and associate with mitotic chromatin. We generated single and double maternal knockout mouse models to deplete maternal stores of Dppa2/4. Importantly, while fertile, Dppa2/4 maternal knockout mice had reduced litter sizes, indicating decreased offspring survival. Immunofluorescence and transcriptome analyses of 2-cell embryos revealed while ZGA took place there were subtle defects in embryos lacking maternal Dppa2/4. Strikingly, heterozygous offspring that inherited the null allele maternally had higher preweaning lethality than those that inherited the null allele paternally. Together our results show that while Dppa2/4 are dispensable for ZGA transcription, maternal stores have an important role in offspring survival, potentially via epigenetic priming of developmental genes.

Cold shock induces a terminal investment reproductive response in C. elegans

Challenges from environmental stressors have a profound impact on many life-history traits of an organism, including reproductive strategy. Examples across multiple taxa have demonstrated that maternal reproductive investment resulting from stress can improve offspring survival; a form of matricidal provisioning when death appears imminent is known as terminal investment. Here we report a reproductive response in the nematode Caenorhabditis elegans upon exposure to acute cold shock at 2°C, whereby vitellogenic lipid movement from the soma to the germline appears to be massively upregulated at the expense of parental survival. This response is dependent on functional TAX-2;TAX-4 cGMP-gated channels that are part of canonical thermosensory mechanisms in worms and can be prevented in the presence of activated SKN-1/Nrf2, the master stress regulator. Increased maternal provisioning promotes improved embryonic cold shock survival, which is notably suppressed in animals with impaired vitellogenesis. These findings suggest that cold shock in C. elegans triggers terminal investment to promote progeny fitness at the expense of parental survival and may serve as a tractable model for future studies of stress-induced progeny plasticity.

Oxytocin neurons enable social transmission of maternal behaviour

Maternal care, including by non-biological parents, is important for offspring survival1–8. Oxytocin1,2,9–15, which is released by the hypothalamic paraventricular nucleus (PVN), is a critical maternal hormone. In mice, oxytocin enables neuroplasticity in the auditory cortex for maternal recognition of pup distress15. However, it is unclear how initial parental experience promotes hypothalamic signalling and cortical plasticity for reliable maternal care. Here we continuously monitored the behaviour of female virgin mice co-housed with an experienced mother and litter. This documentary approach was synchronized with neural recordings from the virgin PVN, including oxytocin neurons. These cells were activated as virgins were enlisted in maternal care by experienced mothers, who shepherded virgins into the nest and demonstrated pup retrieval. Virgins visually observed maternal retrieval, which activated PVN oxytocin neurons and promoted alloparenting. Thus rodents can acquire maternal behaviour by social transmission, providing a mechanism for adapting the brains of adult caregivers to infant needs via endogenous oxytocin.