Age‐related degeneration of the egg‐laying system promotes matricidal hatching in Caenorhabditis elegans

The identification and characterization of age‐related degenerative changes is a critical goal because it can elucidate mechanisms of aging biology and contribute to understanding interventions that promote longevity. Here, we document a novel, age‐related degenerative change in C. elegans hermaphrodites, an important model system for the genetic analysis of longevity. Matricidal hatching—intra‐uterine hatching of progeny that causes maternal death—displayed an age‐related increase in frequency and affected ~70% of mated, wild‐type hermaphrodites. The timing and incidence of matricidal hatching were largely independent of the levels of early and total progeny production and the duration of male exposure. Thus, matricidal hatching appears to reflect intrinsic age‐related degeneration of the egg‐laying system rather than use‐dependent damage accumulation. Consistent with this model, mutations that extend longevity by causing dietary restriction significantly delayed matricidal hatching, indicating age‐related degeneration of the egg‐laying system is controlled by nutrient availability. To identify the underlying tissue defect, we analyzed serotonin signaling that triggers vulval muscle contractions. Mated hermaphrodites displayed an age‐related decline in the ability to lay eggs in response to exogenous serotonin, indicating that vulval muscles and/or a further downstream function that is necessary for egg laying degenerate in an age‐related manner. By characterizing a new, age‐related degenerative event displayed by C. elegans hermaphrodites, these studies contribute to understanding a frequent cause of death in mated hermaphrodites and establish a model of age‐related reproductive complications that may be relevant to the birthing process in other animals such as humans.     

Sex and hatching order modulate the association between MHC‐II diversity and fitness in early‐life stages of a wild seabird

Genes of the major histocompatibility complex (MHC) play a pivotal role in parasite resistance, and their allelic diversity has been associated with fitness variations in several taxa. However, studies report inconsistencies in the direction of this association, with either positive, quadratic or no association being described. These discrepancies may arise because the fitness costs and benefits of MHC diversity differ among individuals depending on their exposure and immune responses to parasites. Here, we investigated in black‐legged kittiwake (Rissa tridactyla) chicks whether associations between MHC class‐II diversity and fitness vary with sex and hatching order. MHC‐II diversity was positively associated with growth and tick clearance in female chicks, but not in male chicks. Our data also revealed a positive association between MHC‐II diversity and survival in second‐hatched female chicks (two eggs being the typical clutch size). These findings may result from condition‐dependent parasite infections differentially impacting sexes in relation to hatching order. We thus suggest that it may be important to account for individual heterogeneities in traits that potentially exert selective pressures on MHC diversity in order to properly predict MHC–fitness associations.     

Climate changes influence free‐living stages of soil‐transmitted parasites of European rabbits

Climate warming has been suggested to augment the risk of infectious disease outbreaks by extending the seasonal window for parasite growth and by increasing the rate of transmission. Understanding how this occurs in parasite‐host systems is important for appreciating long‐term and seasonal changes in host exposure to infection and to reduce species extinction caused by diseases. We investigated how free‐living stages of two soil‐transmitted helminths of the European rabbit (Oryctolagus cuniculus) responded to experimental changes in temperature by performing laboratory experiments with environmental chambers and field manipulations using open‐top‐chambers. This study was motivated by our previous observations that air temperature has increased over the last 30 years in our field site and that during this period intensity of infection of Graphidium strigosum but not Trichostrongylus retortaeformis was positively associated with this temperature increase. Laboratory and field experiments showed that both parasites accelerated egg development and increased hatching rate and larval survival in response to accumulating thermal energy. Both parasites behaved similarly when exposed to diverse temperature regimes, decadal trends, and monthly fluctuations, however, T. retortaeformis was more successful than G. strigosum by showing higher rates of egg hatching and larval survival. Across the months, the first day of hatching occurred earlier in warmer conditions suggesting that climate warming can lengthen the period of parasite growth and host exposure to infective stages. Also, T. retortaeformis hatched earlier than G. strigosum. These findings showed that seasonal changes in intensity, frequency, and duration of daily temperature are important causes of variability in egg hatching and larva survival. Overall, this study emphasizes the important role of climate warming and seasonality on the dynamics of free‐living stages in soil‐transmitted helminths and their contribution to enhance host exposure to parasitic infections. Yet, the ability to infect might ultimately depend on how hosts interact with parasites.     

Host‐specific thermal profiles affect fitness of a widespread pathogen

Host behavior can interact with environmental context to influence outcomes of pathogen exposure and the impact of disease on species and populations. Determining whether the thermal behaviors of individual species influence susceptibility to disease can help enhance our ability to explain and predict how and when disease outbreaks are likely to occur. The widespread disease chytridiomycosis (caused by the fungal pathogen Batrachochytrium dendrobatidis, Bd) often has species‐specific impacts on amphibian communities; some host species are asymptomatic, whereas others experience mass mortalities and population extirpation. We determined whether the average natural thermal regimes experienced by sympatric frog species in nature, in and of themselves, can account for differences in vulnerability to disease. We did this by growing Bd under temperatures mimicking those experienced by frogs in the wild. At low and high elevations, the rainforest frogs Litoria nannotis, L. rheocola, and L. serrata maintained mean thermal regimes within the optimal range for pathogen growth (15–25°C). Thermal regimes for L. serrata, which has recovered from Bd‐related declines, resulted in slower pathogen growth than the cooler and less variable thermal regimes for the other two species, which have experienced more long‐lasting declines. For L. rheocola and L. serrata, pathogen growth was faster in thermal regimes corresponding to high elevations than in those corresponding to low elevations, where temperatures were warmer. For L. nannotis, which prefers moist and thermally stable microenvironments, pathogen growth was fastest for low‐elevation thermal regimes. All of the thermal regimes we tested resulted in pathogen growth rates equivalent to, or significantly faster than, rates expected from constant‐temperature experiments. The effects of host body temperature on Bd can explain many of the broad ecological patterns of population declines in our focal species, via direct effects on pathogen fitness. Understanding the functional response of pathogens to conditions experienced by the host is important for determining the ecological drivers of disease outbreaks.     

Laying‐sequence variation in yolk carotenoids and egg characteristics in the red‐winged blackbird Agelaius phoeniceus

In many bird species with asynchronous hatching, smaller, later‐hatched nestlings are out‐competed for food by their larger, earlier‐hatched siblings and therefore suffer increased mortality via starvation. It is thought that female birds can either maintain or reduce the survival disadvantage of later‐hatched nestlings by differentially allocating maternal resources across the eggs of a clutch. Carotenoid pigments are an example of resources that female birds allocate differentially when producing a clutch, but laying sequence patterns for these pigments remain poorly studied in North American songbirds. We examined intraclutch variation in yolk carotenoids and egg metrics in 27 full clutches of red‐winged blackbird Agelaius phoeniceus eggs collected from eight wetlands in central Alberta, Canada. We predicted that carotenoids would decrease across the laying sequence, as in this species, later‐hatched, marginal nestlings suffer greater mortality than earlier‐hatched, core nestlings. We found nine carotenoid pigments in red‐winged blackbird egg yolks, including two that have never been described from avian yolks: α‐doradexanthin and adonirubin. As predicted, concentrations and amounts of most carotenoids decreased across the laying sequence, suggesting that female red‐winged blackbirds depleted their carotenoid resources as they laid more eggs. However, egg mass and yolk mass both increased across the laying sequence, suggesting that female red‐winged blackbirds may use other maternal resources to compensate for the size and survival disadvantage experienced by later‐hatched, marginal nestlings.     

Effects of host genetics and environment on egg‐associated microbiotas in brown trout (Salmo trutta)

Recent studies found fish egg‐specific bacterial communities that changed over the course of embryogenesis, suggesting an interaction between the developing host and its microbiota. Indeed, single‐strain infections demonstrated that the virulence of opportunistic bacteria is influenced by environmental factors and host immune genes. However, the interplay between a fish embryo host and its microbiota has not been studied yet at the community level. To test whether host genetics affects the assemblage of egg‐associated bacteria, adult brown trout (Salmo trutta) were sampled from a natural population. Their gametes were used for full‐factorial in vitro fertilizations to separate sire from dam effects. In total, 2520 embryos were singly raised under experimental conditions that differently support microbial growth. High‐throughput 16S rRNA amplicon sequencing was applied to characterize bacterial communities on milt and fertilized eggs across treatments. Dam and sire identity influenced embryo mortality, time until hatching and composition of egg‐associated microbiotas, but no link between bacterial communities on milt and on fertilized eggs could be found. Elevated resources increased embryo mortality and modified bacterial communities with a shift in their putative functional potential. Resource availability did not significantly affect any parental effects on embryo performance. Sire identity affected bacterial diversity that turned out to be a significant predictor of hatching time: embryos associated with high bacterial diversity hatched later. We conclude that both host genetics and the availability of resources define diversity and composition of egg‐associated bacterial communities that then affect the life history of their hosts.     

Rainfall variability maintains grass‐forb species coexistence

Environmental variability can structure species coexistence by enhancing niche partitioning. Modern coexistence theory highlights two fluctuation‐dependent temporal coexistence mechanisms —the storage effect and relative nonlinearity – but empirical tests are rare. Here, we experimentally test if environmental fluctuations enhance coexistence in a California annual grassland. We manipulate rainfall timing and relative densities of the grass Avena barbata and forb Erodium botrys, parameterise a demographic model, and partition coexistence mechanisms. Rainfall variability was integral to grass–forb coexistence. Variability enhanced growth rates of both species, and early‐season drought was essential for Erodium persistence. While theoretical developments have focused on the storage effect, it was not critical for coexistence. In comparison, relative nonlinearity strongly stabilised coexistence, where Erodium experienced disproportionately high growth under early‐season drought due to competitive release from Avena. Our results underscore the importance of environmental variability and suggest that relative nonlinearity is a critical if underappreciated coexistence mechanism.     

Within‐female plasticity in sex allocation is associated with a behavioural polyphenism in house wrens

Sex allocation theory assumes individual plasticity in maternal strategies, but few studies have investigated within‐individual changes across environments. In house wrens, differences between nests in the degree of hatching synchrony of eggs represent a behavioural polyphenism in females, and its expression varies with seasonal changes in the environment. Between‐nest differences in hatching asynchrony also create different environments for offspring, and sons are more strongly affected than daughters by sibling competition when hatching occurs asynchronously over several days. Here, we examined variation in hatching asynchrony and sex allocation, and its consequences for offspring fitness. The number and condition of fledglings declined seasonally, and the frequency of asynchronous hatching increased. In broods hatched asynchronously, sons, which are over‐represented in the earlier‐laid eggs, were in better condition than daughters, which are over‐represented in the later‐laid eggs. Nonetheless, asynchronous broods were more productive later within seasons. The proportion of sons in asynchronous broods increased seasonally, whereas there was a seasonal increase in the production of daughters by mothers hatching their eggs synchronously, which was characterized by within‐female changes in offspring sex and not by sex‐biased mortality. As adults, sons from asynchronous broods were in better condition and produced more broods of their own than males from synchronous broods, and both males and females from asynchronous broods had higher lifetime reproductive success than those from synchronous broods. In conclusion, hatching patterns are under maternal control, representing distinct strategies for allocating offspring within broods, and are associated with offspring sex ratios and differences in offspring reproductive success.     

Adaptive difference in daily timing of hatch in two locust species,Schistocerca gregaria and Locusta migratoria: The effects of thermocycles and phase polyphenism

This study examined the effects of temperature and phase polyphenism on egg hatching time in the desert locust, Schistocerca gregaria, and the migratory locust, Locusta migratoria. The two species exhibited differences and similarities in hatching behavior when exposed to different temperature conditions. In 12-h thermocycles of various temperatures, the S. gregaria eggs hatched during the cryoperiod (low temperature period), whereas L. migratoria eggs hatched during the thermoperiod (high temperature period). The eggs of both species hatched during the species-specific period of the thermoperiod in response to a temperature difference as small as 1 °C. Furthermore, the locusts adjusted hatching time to a new thermal environment that occurred shortly before the expected hatching time. In both species, the hatching of the eggs was synchronized to a specific time of the day, and two hatching peaks separated by approximately 1 day were observed at a constant temperature after the eggs were transferred from thermocycles 3 days before hatching. Eggs laid by gregarious females hatched earlier than those laid by solitarious females in S. gregaria but this difference was not observed in L. migratoria.     

Nautilid nurseries: hatchlings and juveniles of Eutrephoceras dekayi from the lower Maastrichtian (Upper Cretaceous) Pierre Shale of east‐central Montana

The nautilid Eutrephoceras dekayi (Morton 1834) is relatively abundant in the lower Maastrichtian (Upper Cretaceous) Pierre Shale of east‐central Montana. We analysed the morphology, size frequency distribution, and isotope composition of a large collection of 220 well‐preserved specimens including hatchlings, juveniles and adults. The newly hatched shell is approximately 14 mm in diameter with a body chamber one‐third whorl in angular length terminating in the nepionic constriction. Internally, the embryonic shell contains five septa. Juveniles are abundant and comprise two‐thirds of the sample whereas sub‐adults, defined by the incipient flattening of the venter, are rare. Adults comprise approximately one‐third of the sample and average 100 mm in diameter. The co‐occurrence of newly hatched shells, small juveniles and adults suggests that the eggs were laid in the same area in which the hatchlings developed. Based on the excellent preservation of the juveniles, we conclude that they did not float into the area after death, but lived in the region, implying that this area served as a nursery for young animals. The calculated temperatures of the embryonic shells are similar to those of the post‐embryonic shells and generally range from 16 to 18 °C. Upon hatching, the nautilids probably followed a demersal mode of life and lived in well‐oxygenated water ≤50 m deep. An examination of lethal injuries (puncture holes) suggests that all ontogenetic stages were equally vulnerable to predation. The proximity of the site to the Sheridan Delta suggests that the specimens were smothered by sudden pulses of sediment transported into the area by major storms.     

Hatching order affects offspring growth,survival and adult dominance in the joint‐laying Pukeko Porphyrio melanotus melanotus

In birds with asynchronous hatching, hatching order is an important factor in determining offspring phenotype. Many previous studies have demonstrated that later‐hatched offspring show reduced growth and survival during development. However, few studies have followed individuals from hatching to adulthood to test whether the effects of hatching order persist into later life. Here, we explore patterns of hatching order and fitness‐related traits in the Pukeko Porphyrio melanotus melanotus, a cooperatively breeding bird that lives in stable social groups that form linear dominance hierarchies. Pukeko groups sometimes contain two breeding females that lay eggs in the same nest (joint‐laying). Thus, competition between nest‐mates can influence the relative fitness of each laying female. We show that in both single‐clutch and joint‐clutch nests, earlier‐hatched Pukeko chicks grow faster and survive better than later‐hatched brood‐mates. Moreover, earlier‐hatched chicks achieve higher dominance ranks as adults, making this study one of the first to find a relationship between hatching order and adult dominance in wild birds. Finally, we show that in groups with two breeding females, the chicks of the primary female hatch earlier than the chicks of the secondary female. As a result, the offspring of the primary female may be at a competitive advantage, which could have important implications for social dynamics in this species.     

Pre‐release risk assessment of the egg‐parasitoid Gryon pennsylvanicum for classical biological control of Leptoglossus occidentalis

Leptoglossus occidentalis Heidemann (Heteroptera: Coreidae) is a North American conifer seed pest that was accidentally introduced to Europe. In the Mediterranean area, it threatens the production of Pinus pinea Linnaeus seeds. The egg‐parasitoid Gryon pennsylvanicum (Ashmead) (Hymenoptera: Platygastridae), the main natural enemy in the native range of L. occidentalis, was imported from British Columbia to Italy. Pre‐release risk assessments were made under quarantine conditions by no‐choice tests conducted with naïve and experienced G. pennsylvanicum offering single eggs of target and non‐target species for varying exposure times (1, 4, 48 h). G. pennsylvanicum successfully parasitized from 75% to 100% of the target host eggs. Only one female specimen of the egg‐parasitoid emerged from a non‐target egg (Gonocerus juniperi Herrich‐Schaeffer, Heteroptera: Coreidae). Two dead female specimens were found, one inside an egg of Coreus marginatus (Linnaeus) (Heteroptera: Coreidae) and one in an egg of Camptopus lateralis (Germar) (Heteroptera: Alydidae). All three cases occurred at the longest oviposition exposure time. Results obtained with this conservative approach suggest that the risk to non‐target species of releasing G. pennsylvanicum in Italy is low.     

Sex,growth rate,rank order after brood reduction,and hatching date affect first‐year survival of long‐lived Herring Gulls

Among most species of birds, survival from hatching throughout the first year of life is generally lower than subsequent survival rates. Survival of young birds during their first year may depend on a combination of selection, learning, unpredictable resources, and environmental events (i.e., post‐fledging factors). However, knowledge about post‐fledging development in long‐lived species is usually limited due to a lengthy immature stage when individuals are generally unobservable. Therefore, pre‐fledging characteristics are often used to predict the survival of young birds. We assessed effects of nestling growth rates, hatching date, hatching asynchrony, brood size and rank order after brood reduction, and sex on first‐year survival of 137 fledglings using a mark‐resighting analysis. We found that the survival probability (Φ_1yr = 0.39) of first‐year Herring Gulls (Larus argentatus) in our study colony located at the outer port of Zeebrugge (Belgium) was lower than that of older individuals (Φ_>1yr = 0.75). All 10 models best supported by our data included nestling growth rate, suggesting that variability in first‐year survival may be linked primarily to individual variation in growth. First‐year survival was negatively correlated with hatching date and rank order after brood reduction. Hence, carry‐over effects of breeding season events such as timing of breeding, early development, and social status had an influence on survival of Herring Gulls after fledging. Furthermore, we found sex‐biased mortality in first‐year Herring Gulls, with females (Φ_1yr = 0.45) surviving better than males (Φ_1yr = 0.38). Although adult survival is generally regarded as the key parameter driving population trajectories in long‐lived species, juvenile survival has recently been acknowledged as an important source of variability in population growth rates. Thus, increasing our knowledge of factors affecting age‐specific survival rates is necessary to improve our understanding of population dynamics and ultimately life‐history variation.     

Direct and transgenerational effects of an experimental heatwave on early life stages in a freshwater snail

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Embryology and early ontogeny of an endemic tooth‐carp fish,Aphanius sophiae (Heckel, 1847)

Understanding embryonic development and ontogeny of species is a crucial part of any further biology, ecology and conservation studies. The present study describes the first detailed normal embryonic development of a tooth‐carp, Aphanius sophiae (Heckel, 1847), from fertilization to post‐ hatching. Aphanius sophiae spontaneously spawned at 24 ± 1°C. The newly laid eggs were transparent and spherical (1.45 ± 0.20 mm). We documented developmental times at 24 ± 1°C to egg activation (0.5 hr), cleavage (3 hr), blastula (10 hr), gastrula (20 hr), neurula (24 hr), somite (28 hr), turnover (60 hr), blood circulation (70 hr) and hatching (330 hr). This study contributes to a further understanding of the embryology and the early ontogeny of A. sophiae and may help improve the culture of other threatened species of the genus Aphanius.     

The effects of different cold‐temperature regimes on development,growth, and susceptibility to an abiotic and biotic stressor

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Ontogenesis and embryogenesis of Megaleporinus elongatus larvae (Characiformes: Anostomidae) from the Jequitinhonha River Basin

Five females and five males of Megaleporinus elongatus captured in the Jequitinhonha River were transferred to hypophysation tanks with a constant water flow at 26°C at the Machado Mineiro Fish Farm. They were submitted to induced reproduction by the hypophysation method. Crude carp pituitary extract (Cyprinus carpio) was injected into the coelomic cavity in two doses (2.5 and 5.0 mg/kg) for males and 3 doses (2.5, 5.0, and 2.5 mg/kg) for females. The doses were applied with a 24‐hr interval between the 1st and 2nd doses and a 12‐hr interval between the 2nd and 3rd ones. Oocytes and semen were obtained by manual extrusion, and the dry method was used for fertilisation. The eggs were kept in funnel type 20‐litre incubators with constant water flow at 23°C. Egg samples were collected every 10 min and photographed under a stereomicroscope for analysis of embryonic development until hatching. The main events of embryogenesis and their respective duration times were: cleavage (45 min), blastula (3 hr 14 min), gastrula (5 hr 25 min), closure of blastopore (6 hr 34 min), differentiation of somites (13 hr 20 min), tail release (17 hr 50 min), and hatching (24 hr 50 min). During the larval ontogenesis, the yolk sac gradually decreased until its complete reabsorption on the 7th day after hatching. The opening of the mouth and digestive tract occurred from the 5th to the 7th day, indicating that larvae could feed exogenously. These results provide information to improve the techniques of induced spawning and cultivation of M. elongatus.     

Low incubation investment in the burrow‐nesting Crab Plover Dromas ardeola permits extended foraging on a tidal food resource

We used GPS data‐loggers, video‐recordings and dummy eggs to assess whether foraging needs may force the low incubation attentiveness (< 55%) of the Crab Plover Dromas ardeola, a crab‐eating wader of the Indian Ocean that nests colonially in burrows. The tidal cycle was the major determinant of the time budget and some foraging trips were more distant from the colony than previously known (up to 26 km away and lasting up to 45 h). The longest trips were mostly made by off‐duty parents, but on‐duty parents also frequently left the nest unattended while foraging for 1–7 h. However, the time spent at the colony area (47%) and the time spent roosting on the foraging grounds (16%) would have allowed almost continuous incubation, as in other species with shared incubation. Therefore, the low incubation attentiveness is not explained by the need for long foraging trips but is largely dependent on a high intermittent rhythm of incubation with many short recesses (5.8 ± 2.6 recesses/h) that were not spent foraging but just outside the burrow or thermoregulating at the seashore. As a result, the eggs were warmed on average only 1.7 °C above burrow temperature, slightly more during high tide periods and when burrow temperature was lower between 20:00 and 10:00 h, only partly counteracting the temperature fluctuations of the incubation chamber. These results suggest that low incubation attentiveness is due to the favourable thermal conditions provided by safe nesting burrows and by the hot tropical breeding season, a combination that allows simultaneous foraging by parents and the exploitation of distant foraging grounds. Why Crab Plovers engage in many short recesses from incubation still remains to be clarified but the need to thermoregulate at the seashore and to watch for predators may play a role.     

Differences in egg size, shell thickness, pore density, pore diameter and water vapour conductance between first and second eggs of Snares Penguins Eudyptes robustus and their influence on hatching asynchrony

Brood reduction in birds is frequently induced by hatching asynchrony. Crested penguins (genus Eudyptes) are obligate brood reducers, but in contrast to most other birds, first‐laid eggs are considerably smaller in size than second‐laid eggs; furthermore, first‐laid eggs hatch after their siblings. The mechanisms underlying this reversal in size and hatching order remain unclear. In this study, we tested whether the second‐laid eggs of Snares Penguins Eudyptes robustus have a higher eggshell porosity allowing them to maintain a higher metabolic rate throughout incubation and to hatch before their first‐laid siblings. We investigated differences in egg size, shell thickness, pore density, pore diameter and water vapour conductance between first and second eggs within clutches and examined the influence of these shell characteristics on hatching asynchrony. First‐laid eggs of Snares Penguins were approximately 78% of the size of the larger second eggs. Second‐laid eggs had considerably thicker shells and more pores per cm² than first eggs, whereas pore diameter did not differ between eggs. Water vapour conductance was greater in second‐ (16.8 mg/day/torr) than in first‐laid eggs (14.9 mg/day/torr). The difference in water vapour conductance between first‐ and second‐laid eggs within clutches was related to hatching patterns. In nests where second eggs hatched before first‐laid eggs, second eggs had a considerably greater water conductance than their sibling, whereas in nests where both eggs hatched on the same day, the difference in water conductance between eggs was very small, and in a few nests where small first eggs hatched before their larger sibling, they had a greater water conductance than their larger second‐laid nestmate. Surprisingly few studies have investigated differences in shell characteristics between eggs within clutches and associated effects on hatching asynchrony. This study has demonstrated that such differences exist between eggs within clutches and that they can influence hatching patterns.