Maternal effect senescence via reduced DNA repair ability in the three-spined stickleback.

Maternal effect senescence, a decline in offspring viability with maternal age, has been documented across diverse animals, but its mechanisms remain largely unknown. Here, we test maternal effect senescence and explore its possible molecular mechanisms in a fish. We compared the levels of maternal mRNA transcripts of DNA repair genes and mtDNA copies in eggs and the levels of DNA damage in somatic and germline tissues between young and old female sticklebacks. We also tested, in an in vitro fertilization experiment, whether maternal age and sperm DNA damage level interactively influence the expression of DNA repair genes in early embryos. Old females transferred less mRNA transcripts of DNA repair genes into their eggs than did young females, but maternal age did not influence egg mtDNA density. Despite a higher level of oxidative DNA damage in the skeletal muscle, old females had a similar level of damage in the gonad to young females, suggesting the prioritization for germline maintenance during ageing. The embryos of both old and young mothers increased the expression of DNA repair genes in response to an increased level of oxidative DNA damage in sperm used for their fertilization. The offspring of old mothers showed higher rates of hatching, morphological deformity and post-hatching mortality and had smaller body size at maturity. These results suggest that maternal effect senescence may be mediated by reduced capacity of eggs to detect and repair DNA damages, especially prior to the embryonic genomic activation.

A variable refractory period increases collective performance in noisy environments.

Synchronized oscillations are found in all living systems, from cellsto ecosystems and on varying time scales. A generic principlebehind the production of oscillations involves a delay in theresponse of one entity to stimulations from the others in the sys-tem. Communication among entities is required for the emergenceof synchronization, but its efficacy can be impaired by surroundingnoise. In the social spiderAnelosimus eximius, individuals coordi-nate their activity to catch large prey that are otherwise inaccessi-ble to solitary hunters. When hunting in groups, dozens of spidersmove rhythmically toward their prey by synchronizing movingand stopping phases. We proposed a mechanistic model imple-menting individual behavioral rules, all derived fromfield experi-ments, to elucidate the underlying principles of synchronization.We showed that the emergence of oscillations in spiders involvesa refractory state, the duration of which depends on the relativeintensity of prey versus conspecific signals. Thisflexible behaviorallows individuals to rapidly adapt to variations in their vibrationallandscapes. Exploring the model reveals that the benefits of syn-chronization resulting from improved accuracy in prey detectionand reduced latency to capture prey more than offset the cost ofthe delay associated with immobility phases. Overall, our studyshows that a refractory period whose duration is variable anddependent on information accessible to all entities in the systemcontributes to the emergence of self-organized oscillations innoisy environments. Ourfindings may inspire the design of artifi-cial systems requiring fast andflexible synchronization betweentheir components.

Mitochondrial DNA content in eggs as a maternal effect.

The transmission of detrimental mutations in animal mitochondrial DNA (mtDNA) to the next generation is avoided by a high level of mtDNA content in mature oocytes. Thus, this maternal genetic material has the potential to mediate adaptive maternal effects if mothers change mtDNA level in oocytes in response to their environment or body condition. Here, we show that increased mtDNA abundance in mature oocytes was associated with fast somatic growth during early development but at the cost of increased mortality in three-spined sticklebacks. We also examined whether oocyte mtDNA and sperm DNA damage levels have interacting effects because they can determine the integrity of mitochondrial and nuclear genes in offspring. The level of oxidative DNA damage in sperm negatively affected fertility, but there was no interacting effect of oocyte mtDNA abundance and sperm DNA damage. Oocyte mtDNA level increased towards the end of the breeding season, and the females exposed to warmer temperatures during winter produced eggs with increased mtDNA copies. Our results suggest that oocyte mtDNA level can vary according to the expected energy demands for offspring during embryogenesis and early growth. Thus, mothers can affect offspring development and viability through the context-dependent effects of oocyte mtDNA abundance.

Relationships between male secondary sexual traits, physiological state and offspring viability in the three-spined stickleback.

BACKGROUND: Sexual signals produced by males play a central role in sexual selection, but the relationship between these traits and the quality of the bearer are often ambiguous. Secondary sexual traits may represent genetic quality of the bearer, resulting in positive relationships with physiological state, or may be costly to produce, showing trade-off with physiological state. A number of studies have explored the relationships between secondary sexual traits and other functional traits, but few have studied their fitness consequences. We studied the link between diverse physiological traits and both morphological and behavioural sexual traits and examined how their interplay influences offspring viability in the three-spined stickleback. RESULTS: Male sticklebacks showing nest building and courtship behaviour were smaller than those not investing in reproductive activities. There was no evidence that the expression of red nuptial colouration and the quality of courtship behaviour of males are positively related to their metabolic rates, swim ability, oxidative damage and mtDNA copy number. However, individuals showing larger red nuptial colour areas had higher levels of oxidative DNA damage in their sperm. Male courtship behaviour and aggressiveness, but not red colour area, were good predictors of offspring hatching and survival. CONCLUSIONS: Our results suggest that, in our study population at the southern edge of the species' distribution, sexual colouration of male sticklebacks was not a good indicator of their body state, but both courtship quality and aggressiveness during the courtship are reliable cues of their gamete quality, influencing the viability of their offspring. Thus, females that choose mates based on their courtship behaviour will have high fitness. In the study population, which represents a fast pace-of-life with high reproductive rate and short lifespan, sexual ornaments of males may not honestly signal their physiological and physical state because they invest at maximum in a single reproductive season despite high costs.

Trap versus net: Behavioural sampling bias caused by capture method in three-spined sticklebacks.

Wild-caught animals are often used in behavioural or other biological studies. However, different capture methods may target individuals that differ in behaviour, life history and morphology, thereby giving rise to sampling biases. Here, we investigated whether juvenile three-spined sticklebacks caught in a natural population by passive and active sampling methods using frequently used tools (i.e. trap and hand net) differ in behaviours related to cognition and personality. The fish caught by traps were more prone to take risks and shoal (i.e. bolder and more sociable), but smaller in size and mass than the fish caught by hand nets. Individual variation in boldness was greater in the fish caught by hand nets, suggesting that this active sampling method may capture more representative samples of the natural population. Our results show the importance of capture method to avoid sampling bias in behavioural studies using wild-caught animals.

Social intolerance is a consequence, not a cause, of dispersal in spiders.

From invertebrates to vertebrates, a wealth of species display transient sociality during their life cycle. Investigating the causes of dispersal in temporary associations is important to better understand population dynamics. It is also essential to identify possible mechanisms involved in the evolutionary transition from transient to stable sociality, which has been documented repeatedly across taxa and typically requires the suppression of dispersal. In many animals, the onset of dispersal during ontogeny coincides with a sharp decline in social tolerance, but the causal relationship still remains poorly understood. Spiders offer relevant models to explore this question, because the adults of the vast majority of species (>48,000) are solitary and aggressive, but juveniles of most (if not all) species are gregarious and display amicable behaviors. We deployed a combination of behavioral, chemical, and modelling approaches in spiderlings of a solitary species to investigate the mechanisms controlling the developmental switch leading to the decline of social cohesion and the loss of tolerance. We show that maturation causes an increase in mobility that is sufficient to elicit dispersal without requiring any change in social behaviors. Our results further demonstrate that social isolation following dispersal triggers aggressiveness in altering the processing of conspecifics' cues. We thus provide strong evidence that aggression is a consequence, not a cause, of dispersal in spiderlings. Overall, this study highlights the need of extended social interactions to preserve tolerance, which opens new perspectives for understanding the routes to permanent sociality.

Age and egg-sac loss determine maternal behaviour and locomotor activity of wolf spiders (Araneae, Lycosidae).

Wolf spiders' (Lycosidae) maternal behaviour includes a specific phase called "egg brooding" which consists of guarding and carrying an egg-sac throughout the incubation period. The transport of an egg-sac can restrict mothers' exploratory and locomotor activity, in particular when foraging. The present study details the ontogeny of maternal behaviour and assesses the influence of age of egg-sac (or embryos' developmental stage) on vagrant wolf spider Pardosa saltans females' exploration and locomotion. We observed these spiders' maternal behaviour in the laboratory and evaluated their locomotor activity using a digital activity recording device. Our subjects were virgin females (without egg-sac) and first time mothers (with her egg-sac) who were divided into three groups. The first group of mothers were tested on the day the egg-sac was built (day 0), and the females of the other two groups were tested 10 or 15days after they had built their egg-sac. We evaluated the effects of the presence and the loss of egg-sac on mothers' activity. Pardosa saltans females' behaviour depended on mothers' physiological state and/or age of egg-sac (developmental stage of embryos). Virgin females' behaviour was not modified by the presence of an egg-sac in their environment. Mothers' reactions to the presence, the loss and the recovery of their egg-sac varied during the maternal cycle. Maternal behaviour changed with age of egg-sac, but the levels of locomotor activity of mothers with egg-sacs was similar to those of virgin females. Loss of egg-sac modified the maternal behaviour and locomotor activity of all mothers; these modifications were greater on "day 15" when embryos had emerged from eggs. All mothers were able to retrieve their egg-sacs and to re-attach them to their spinnerets.