Parental effects on the larval performance of a tapeworm in its copepod first host

Parents can influence the phenotype of their offspring through various mechanisms, besides the direct effect of heredity. Such parental effects are little explored in parasitic organisms, perhaps because in many parasites, per capita investment into offspring is low. I investigated whether parental identity, beyond direct genetic effects, could explain variation in the performance of the tapeworm Schistocephalus solidus in its first intermediate host, a copepod. I first determined that two breeding worms could be separated from one another after ~48 h of in vitro incubation and that the isolated worms continued producing outcrossed eggs, that is, rates self‐fertilization did not increase after separation. Thus, from a breeding pair, two sets of genetically comparable eggs can be collected that have unambiguous parental identities. In an infection experiment, I found that the development of larval worms tended to vary between the two parental worms within breeding pairs, but infection success and growth rate in copepods did not. Accounting for this parental effect decreased the estimated heritability for development by nearly half. These results suggest that larval performance is not simply a function of a worm's genotype; who mothered or fathered an offspring can also affect offspring fitness, contradicting the perhaps naïve idea that parasites simply produce large quantities of uniformly low‐quality offspring.     

A limit on the extent to which increased egg size can compensate for a poor postnatal environment revealed experimentally in the burying beetle,Nicrophorus vespilloides

It is often assumed that there is a positive relationship between egg size and offspring fitness. However, recent studies have suggested that egg size has a greater effect on offspring fitness in low‐quality environments than in high‐quality environments. Such observations suggest that mothers may compensate for poor posthatching environments by increasing egg size. In this paper we test whether there is a limit on the extent to which increased egg size can compensate for the removal of posthatching parental care in the burying beetle, Nicrophorus vespilloides. Previous experiments with N. vespilloides suggest that an increased egg size can compensate for a relatively poor environment after hatching. Here, we phenotypically engineered female N. vespilloides to produce large or small eggs by varying the amount of time they were allowed to feed on the carcass as larvae. We then tested whether differences between these groups in egg size translated into differences in larval performance in a harsh postnatal environment that excluded parental care. We found that females engineered to produce large eggs did not have higher breeding success, and nor did they produce larger larvae than females engineered to produce small eggs. These results suggest that there is a limit on the extent to which increased maternal investment in egg size can compensate for a poor posthatching environment. We discuss the implication of our results for a recent study showing that experimental N. vespilloides populations can adapt rapidly to the absence of posthatching parental care.     

Mortality of Apatania fimbriata (Insecta: Trichoptera) during embryonic, larval and adult life stages

1. Egg masses, oviposition site preferences, and abiotic and biotic factors causing mortality during embryonic, larval and adult life stages of Apatania fimbriata were studied. Laboratory investigations provided information on the temperature dependence of embryonic development, measured as an increase in egg volume.
2. A. fimbriata laid hemispherical egg masses, consisting of a transparent matrix containing a mean of 208 eggs. Egg masses were laid on stones situated just above the water surface in dark cavities in the stream bank.
3. Two hundred egg masses were mapped and individually monitored during embryonic development. There was no significant correlation between mortality during embryonic development and any of the abiotic parameters measured. First-instar larvae of Osmylus fulvicephalus consumed developing eggs, and chironomids preyed on newly hatched larvae.
4. A mean of seventy-two females emerged per metre of stream. Mortality during the 1993/94 life cycle was measured as a percentage of the potential number of eggs laid. Female mortality between emergence and oviposition was ≈ 80%. Eight per cent of individuals were lost during embryonic development. Larval mortality to emergence in 1994 was 11.3%. This indicates that the terrestrial life stage is probably decisive in the regulation of A. fimbriata populations.
5. Duration of embryogenesis at constant temperatures (4–20 °C) in the laboratory was described best by a negative exponential function. This species is cold stenothermal and there was no hatching success at 20 °C.
6. Egg volumes during embryonic development increased sigmoidally over time.     

Mortality of Apatania fimbriata (Insecta: Trichoptera) during embryonic, larval and adult life stages

1. Egg masses, oviposition site preferences, and abiotic and biotic factors causing mortality during embryonic, larval and adult life stages of Apatania fimbriata were studied. Laboratory investigations provided information on the temperature dependence of embryonic development, measured as an increase in egg volume.
2. A. fimbriata laid hemispherical egg masses, consisting of a transparent matrix containing a mean of 208 eggs. Egg masses were laid on stones situated just above the water surface in dark cavities in the stream bank.
3. Two hundred egg masses were mapped and individually monitored during embryonic development. There was no significant correlation between mortality during embryonic development and any of the abiotic parameters measured. First-instar larvae of Osmylus fulvicephalus consumed developing eggs, and chironomids preyed on newly hatched larvae.
4. A mean of seventy-two females emerged per metre of stream. Mortality during the 1993/94 life cycle was measured as a percentage of the potential number of eggs laid. Female mortality between emergence and oviposition was ≈ 80%. Eight per cent of individuals were lost during embryonic development. Larval mortality to emergence in 1994 was 11.3%. This indicates that the terrestrial life stage is probably decisive in the regulation of A. fimbriata populations.
5. Duration of embryogenesis at constant temperatures (4–20 °C) in the laboratory was described best by a negative exponential function. This species is cold stenothermal and there was no hatching success at 20 °C.
6. Egg volumes during embryonic development increased sigmoidally over time.     

A test of the preference–performance hypothesis with stream insects: selective oviposition affects the hatching success of caddisfly eggs

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Geographical variation in offspring size effects across generations

Offspring size is thought to strongly affect offspring fitness and many studies have shown strong offspring size/fitness relationships in marine and terrestrial organisms. This relationship is strongly mitigated by local environmental conditions and the optimal offspring size that mothers should produce will vary among different environments. It is assumed that offspring size will consistently affect the same traits among populations but this assumption has not been tested. Here I use a common garden experiment to examine the effects of offspring size on subsequent performance for the marine bryozoan Bugula neritina using larvae from two very different populations. The local conditions at one population (Williamstown) favour early reproduction whereas the other population (Pt. Wilson) favours early growth. Despite being placed in the same habitat, the effects of parental larval size were extremely variable and crossed generations. For larvae from Williamstown, parental larval size positively affected initial colony growth and larval size in the next generation. For larvae from the other population, parental larval size positively affected colony fecundity and negatively affected larval size in the next generation. Traditionally, exogenous factors have been viewed as the sole source of variation in offspring size/fitness relationship but these results show that endogenous factors (maternal source population) can also cause variation in this crucial relationship. It appears offspring size effects can be highly variable among populations and organisms can adapt to local conditions without changing the size of their offspring.     

Intrinsic post‐ejaculation sperm ageing does not affect offspring fitness in Atlantic salmon

Post‐meiotic sperm ageing, both before ejaculation and after ejaculation, has been shown to negatively affect offspring fitness by lowering the rate of embryonic development, reducing embryonic viability and decreasing offspring condition. These negative effects are thought to be caused by intrinsic factors such as oxidative stress and ATP depletion or extrinsic factors such as temperature and osmosis. Effects of post‐ejaculation sperm ageing on offspring fitness have so far almost exclusively been tested in internal fertilizers. Here, we tested whether intrinsic post‐ejaculation sperm ageing affects offspring performance in an external fertilizer, the Atlantic salmon Salmo salar. We performed in vitro fertilizations with a split‐clutch design where sperm were subjected to four post‐ejaculation ageing treatments. We varied the duration between sperm activation and fertilization while minimizing extrinsic stress factors and tested how this affected offspring fitness. We found no evidence for an effect of our treatments on embryo survival, hatching time, larval standard length, early larval survival or larval growth rate, indicating that intrinsic post‐ejaculation sperm ageing may not occur in Atlantic salmon. One reason may be the short life span of salmon sperm after ejaculation. Whether our findings are true in other external fertilizers with extended sperm activity remains to be tested.     

Offspring fitness and the optimal propagule size in a fluctuating environment

Propagule size is an important maternal effect on offspring fitness and phenotype in birds and other oviparous animals. The performance of propagules often increases with size, but a fluctuating environment may introduce temporal variation in the optimal phenotype. Understanding these mechanisms will provide novel insights into the eco‐evolutionary dynamics of life history strategies in parental reproductive investment. We investigated the interaction between propagule size (measured as egg volume) and environmental conditions on offspring mortality and phenotype in a Norwegian house sparrow population. Increased propagule size reduced offspring mortality in early life, with more pronounced effects under heavy precipitation. However, the optimal propagule size for low offspring mortality until recruitment shifted from large to small as temperature increased. Propagule size had no significant effect on fledgling body mass and tarsus length. These results reveal a potential for eco‐evolutionary dynamics in propagule size, as populations adapt to fluctuating environmental conditions. The ultimate outcome of this dynamic process will also depend on variation in parental fitness and tradeoffs with other life‐history traits, particularly clutch size.     

Genetic benefits of extreme sequential polyandry in a terrestrial‐breeding frog

Sequential polyandry may evolve as an insurance mechanism to reduce the risk of females choosing mates who are genetically inferior (intrinsic male quality hypothesis) or genetically incompatible (genetic incompatibility hypothesis). The prevalence of such indirect benefits remains controversial, however, because studies estimating the contributions of additive and nonadditive sources of genetic variation to offspring fitness have been limited to a small number of taxonomic groups. Here, we used artificial fertilization techniques combined with a crossclassified breeding design (North Carolina Type II) to simultaneously test the “good genes hypothesis” and the “genetic incompatibility hypothesis” in the brown toadlet (Pseudophryne bibronii); a terrestrial‐breeding species with extreme sequential polyandry. Our results revealed no significant additive or nonadditive genetic effects on fertilization success. Moreover, they revealed no significant additive genetic effects, but highly significant nonadditive genetic effects (sire by dam interaction effects), on hatching success and larval survival to initial and complete metamorphosis. Taken together, these results indicate that offspring viability is significantly influenced by the combination of parental genotypes, and that negative interactions between parental genetic elements manifest during embryonic and larval development. More broadly, our findings provide quantitative genetic evidence that insurance against genetic incompatibility favors the evolution and maintenance of sequential polyandry.     

Fitness consequences of parental compatibility in the frog Crinia georgiana

Theory suggests that multiple mating by females can evolve as a mechanism for acquiring compatible genes that promote offspring fitness. Genetic compatibility models predict that differences in fitness among offspring arise from interactions between male and female haplotypes. Using a cross-classified breeding design and in vitro fertilization, we raised families of maternal and paternal half-siblings of the frog Crinia georgiana, a species with a polyandrous breeding system and external fertilization. After controlling for variation in maternal provisioning, we found significant effects of interacting parental haplotypes on fertilization success, and nonadditive genetic effects on measures of offspring fitness such as embryo survival, and survival to, size at, and time to metamorphosis. Additive genetic variation due to males and females was negligible, and not statistically significant for any of the fitness traits measured. Combinations of parental haplotypes that resulted in high rates of fertilization produced offspring with higher embryo survival and rapid juvenile development. We suggest that a gamete recognition mechanism for selective fertilization by compatible sperm may promote offspring fitness in this system.     

Links between parental life histories of wild salmon and the telomere lengths of their offspring

The importance of parental contributions to offspring development and subsequent performance is self‐evident at a genomic level; however, parents can also affect offspring fitness by indirect genetic and environmental routes. The life history strategy that an individual adopts will be influenced by both genes and environment; and this may have important consequences for offspring. Recent research has linked telomere dynamics (i.e., telomere length and loss) in early life to future viability and longevity. Moreover, a number of studies have reported a heritable component to telomere length across a range of vertebrates, although the effects of other parental contribution pathways have been far less studied. Using wild Atlantic salmon with different parental life histories in an experimental split‐brood in vitro fertilization mating design and rearing the resulting families under standardized conditions, we show that there can be significant links between parental life history and offspring telomere length (studied at the embryo and fry stage). Maternal life history traits, in particular egg size, were most strongly related to offspring telomere length at the embryonic stage, but then became weaker through development. In contrast, paternal life history traits, such as the father's growth rate in early life, had a greater association in the later stages of offspring development. However, offspring telomere length was not significantly related to either maternal or paternal age at reproduction, nor to paternal sperm telomere length. This study demonstrates both the complexity and the importance of parental factors that can influence telomere length in early life.     

Sexual dimorphism,survival, and parental investment in relation to offspring sex in a precocial bird

Differential growth rate between males and females, owing to a sexual size dimorphism, has been proposed as a mechanism driving sex‐biased survival. How parents respond to this selection pressure through sex ratio manipulation and sex‐biased parental investment can have a dramatic influence on fitness. We determined how differential growth rates during early life resulting from sexual size dimorphism affected survival of young and how parents may respond in a precocial bird, the black brant Branta bernicla nigricans. We hypothesized that more rapidly growing male goslings would suffer greater mortality than females during brood rearing and that parents would respond to this by manipulating their primary sex ratio and parental investment. Male brant goslings suffered a 19.5% reduction in survival relative to female goslings and, based on simulation, we determined that a female biased population sex ratio at fledging was never overcome even though previous work demonstrated a slight male‐biased post‐fledging survival rate. Contrary to the Fisherian sex ratio adjustment hypothesis we found that individual adult female brant did not manipulate their primary sex ratio (50.39% male, n = 645), in response to the sex‐biased population level sex ratio. However, female condition at the start of the parental care period was a good predictor of their primary sex ratio. Finally, we examined how females changed their behavior in response to primary sex ratio of their broods. We hypothesized that parents would take male biased broods to areas with increased growth rates. Parents with male biased primary sex ratios took broods to areas with higher growth rates. These factors together suggest that sex‐biased growth rates during early life can dramatically affect population dynamics through sex‐biased survival and recruitment which in turn affects decisions parents make about sex allocation and sex‐biased parental investment in offspring to maximize fitness.     

Unpredictable offspring survivorship in the damselfly, Megaloprepus coerulatus, shapes parental behavior, constrains sexual selection, and challenges traditional fitness estimates

Evolutionary biologists typically assume that the number of eggs fertilized or developing embryos produced is correlated with an individual's fitness. Using microsatellite markers, we document for the first time estimates of realized fitness quantified as the number of offspring surviving to adulthood in an insect under field conditions. In a territorial damselfly whose males defend tree hole oviposition sites, patterns of offspring survivorship could not be anticipated by adults. Fewer than half of the parents contributing eggs to a larval habitat realized any reproductive success from their investment. The best fitness correlate was the span over which eggs in a clutch hatched. Among parents, female fecundity and male fertilization success were poor predictors of realized fitness. Although body size was correlated with female clutch size and male mating success, larger parents did not realize greater fitness than smaller ones. The uncoupling of traditional fitness surrogates from realized fitness provides strong empirical evidence that selection at the larval stage constrains selection on mated adults.     

Size‐dependent reproductive success of wild zebrafish Danio rerio in the laboratory

Size‐dependent reproductive success of wild zebrafish Danio rerio was studied under controlled conditions in the laboratory to further understand the influence of spawner body size on reproductive output and egg and larval traits. Three different spawner size categories attained by size‐selective harvesting of the F₁‐offspring of wild D. rerio were established and their reproductive performance compared during a 5 day period. As to be expected, large females spawned more frequently and had significantly greater clutch sizes than small females. Contrary to expectations, small females produced larger eggs when measured as egg diameter with similar amounts of yolk compared to eggs spawned by large spawners. Eggs from small fish, however, suffered from higher egg mortality than the eggs of large individuals. Embryos from small‐sized spawners also hatched later than offspring from eggs laid by large females. Larval standard length (L_S)‐at‐hatch did not differ between the size categories, but the offspring of the large fish had significantly larger area‐at‐hatch and greater yolk‐sac volume indicating better condition. Offspring growth rates were generally similar between offspring from all size categories, but they were significantly higher for offspring spawned by small females in terms of L_S between days 60 and 90 post‐fertilization. Despite temporarily higher growth rates among the small fish offspring, the smaller energy reserves at hatching translated into lower condition later in ontogeny. It appeared that the influence of spawner body size on egg and larval traits was relatively pronounced early in development and seemed to remain in terms of condition, but not in growth, after the onset of exogenous feeding. Further studies are needed to explore the mechanisms behind the differences in offspring quality between large‐ and small‐sized spawners by disentangling size‐dependent maternal and paternal effects on reproductive variables in D. rerio.     

The more the better – polyandry and genetic similarity are positively linked to reproductive success in a natural population of terrestrial salamanders (Salamandra salamandra)

Although classically thought to be rare, female polyandry is widespread and may entail significant fitness benefits. If females store sperm over extended periods of time, the consequences of polyandry will depend on the pattern of sperm storage, and some of the potential benefits of polyandry can only be realized if sperm from different males is mixed. Our study aimed to determine patterns and consequences of polyandry in an amphibian species, the fire salamander, under fully natural conditions. Fire salamanders are ideal study objects, because mating, fertilization and larval deposition are temporally decoupled, females store sperm for several months, and larvae are deposited in the order of fertilization. Based on 18 microsatellite loci, we conducted paternity analysis of 24 female‐offspring arrays with, in total, over 600 larvae fertilized under complete natural conditions. More than one‐third of females were polyandrous and up to four males were found as sires. Our data clearly show that sperm from multiple males is mixed in the female's spermatheca. Nevertheless, paternity is biased, and the most successful male sires on average 70% of the larvae, suggesting a ‘topping off’ mechanism with first‐male precedence. Female reproductive success increased with the number of sires, most probably because multiple mating ensured high fertilization success. In contrast, offspring number was unaffected by female condition and genetic characteristics, but surprisingly, it increased with the degree of genetic relatedness between females and their sires. Sires of polyandrous females tended to be genetically similar to each other, indicating a role for active female choice.     

Parental effects on fertilization and hatching success and development of Atlantic halibut (Hippoglossus hippoglossus L.) embryos and larvae

The parental effects on fertilization and early life history traits were studied in Atlantic halibut, Hippoglossus hippoglossus L. Sperm from 12 different males were used to fertilize eggs of two females in separate crosses. The fertilization success were generally high, above 80% of developing embryos at 16-cell stage in 20 of 24 crosses with an average of 85.9+/-17.6% and 87.2+/-16.5% for female A and female B, respectively. Corresponding hatching success was 74.8+/-17.7% and 41.6+/-20.1%, respectively. The relationship between fertilization success and hatching success was positive. The parental influence on hatching was dominated by a strong and significant (p<0.001) maternal effect; however, the paternal effect was also significant (p<0.001). Furthermore, there was no relationship between fertilization success, hatching success and larvae viability as a high number of larvae developed locked jaws (i.e., were not functional). There was a significant (p<0.01) difference in yield of functional larvae of female A (43%) and female B (56%), and also between crosses sired by different males. The standard length of offspring of female A (12.4+/-0.5 mm) and B (12.6+/-0.6 mm) were significantly (p<0.001) different, and also significantly influenced by both the female (p<0.001) and the male (p<0.001). The present paper provides strong indications that not only the female, but also the male parent influences quantitative features of early development of their offspring.     

Larval population density affects female weight and fecundity in the dung beetle Aphodius ater

1. Competition for food at high densities during larval development leads to reduced adult weight in the northern temperate dung beetle Aphodius ater. 2. Analysis of female beetles caught in the field showed that numbers of eggs and total egg load per female were correlated positively with beetle size. 3. Female beetles reared at different population densities during larval development in the laboratory were analysed with regard to their lifetime fecundity and reproductive lifespan. 4. High population densities during development had a negative influence on the number of eggs per female and on reproductive lifespan. Lifetime fecundity was correlated positively with female weight. 5. It was concluded that competition during larval development in the first generation of offspring will result in a lower number of offspring in the second generation in Aphodius ater, and thereby reduce parental fitness.     

Survival for specific life intervals of smallmouth bass, Micropterus dolomieu, during parental care

We tested whether daily mortality rates (DMR) of smallmouth bass offspring were influenced by life interval, offspring density and growth, parental male attributes, and selected mortality factors during parental care in a regulated Virginia stream. Mortality averaged 9.5% per day (range 5.2–13.9%) and 94.1% total (range 80.9–99.5%) from egg deposition to the juvenile period (29–36 d) for individual broods. Offspring losses were primarily attributed to fungus (Saprolegnia parasitica) infection of eggs and to American eel, Anguilla rostrata, predation. DMR were significantly higher for the interval from swim-up of larvae to metamorphosis relative to earlier and later intervals. There was no significant autocorrelation of DMR among life intervals for individual broods, indicating that relative mortality rates were inconsistent among broods through time. DMR were also uncorrelated with the number of offspring per brood, offspring growth rates, and parental male attributes, except during egg and embryo intervals. Daily egg mortality was negatively related to male size and positively related to the number of eggs per nest, suggesting that density-dependent egg mortality may have been partially offset in nests of larger males. Larger males received more eggs, tended to maintain larger broods throughout parental care, and contributed a high proportion of the total number of juveniles reared. This revised version was published online in August 2006 with corrections to the Cover Date.     

Elevated water temperature impairs fertilization and embryonic development of whitefish Coregonus lavaretus

The adverse effects of high temperatures on the early life stages of anadromous whitefish Coregonus lavaretus were experimentally examined by assessing fertilization success, the percentage of developmental abnormalities, cumulative mortality and the rate of embryogenesis across a range of temperatures. Temperatures ≥ 7° C increased the proportion of unfertilized and abnormally dividing eggs, deformed embryos and consequent mortality. The higher the temperature, the more severe were the effects. When eggs were fertilized and constantly incubated at various temperatures, the effective level for 50% of the eggs and embryos (EL50) of temperature was 7·6° C at the developmental stage when eye pigmentation was visible. Fewer developmental abnormalities and a lower cumulative mortality rate were observed when embryos were exposed to high temperatures from the later, gastrula stage, than from fertilization or the four‐cell stage. Irrespective of retarded development in terms of day‐degrees (i.e. the sum of daily mean temperatures), a high incubation temperature reduced the development time of C. lavaretus, leading to earlier hatching, and hatched fry were shorter than at the reference temperature of 4–5° C. Global warming will particularly pose risks for stenothermic species such as C. lavaretus, with early life stages being especially susceptible. Thus, relatively small increases and fluctuations in river water temperatures during the spawning season of this anadromous species may have substantial negative impacts on its recruitment and population persistence.     

Why Life Histories Evolve Differently in the Sea

Marine life histories differ from terrestrial life historiesbecause seawater is denser and more viscous than air, becausedesiccation is not a problem for organisms in water, and becausefood is abundant in suspension and solution. (1) Mating andcompetition for paternity in the sea often differs. Female gametesare often spawned freely. Passively dispersed spermatophorescould in some cases provide single paternity to an entire clutchof offspring. Penises of sessile animals reach far for copulation.There are no pollinators. (2) In many clades of benthic marineanimals, greater dispersal of offspring is associated with largeadult size, and greater parental care of offspring and reducedplanktonic larval periods are associated with small adult size.(3) Many benthic marine animals are colonies with modular construction,and these also commonly brood embryos and have short-lived larvae,in contrast to related solitary forms. (4) Unlike dispersalof terrestrial animals, larval dispersal of marine animals isoften obligate with sexual reproduction and often includes aprecompetent period during which larvae cannot settle at goodsites. Unlike terrestrial seeds, marine larvae have no clearadaptations for dispersal, often grow during dispersal, andoften leave bad sites. Feeding planktonic larvae are commonamong marine animals and rare among other aquatic animals, perhapsbecause of persistent aquatic routes between habitable sitesfor marine animals. Peculiarities in marine life histories mayinfluence many aspects of evolution in the sea. Closely relatedsedentary marine animals can differ greatly in larval dispersalwith consequences for recruitment to populations, genetic exchangebetween benthic populations, adaptation to local conditions,sex allocation, interaction with kin, speciation, and extinction.