Predator-induced transgenerational plasticity of parental care behaviour in male three-spined stickleback fish across two generations.

Parental care is a critical determinant of offspring fitness, and parents adjust their care in response to ecological challenges, including predation risk. The experiences of both mothers and fathers can influence phenotypes of future generations (transgenerational plasticity). If it is adaptive for parents to alter parental care in response to predation risk, then we expect F1 and F2 offspring who receive transgenerational cues of predation risk to shift their parental care behaviour if these ancestral cues reliably predict a similarly risky environment as their F0 parents. Here, we used three-spined sticklebacks (Gasterosteus aculeatus) to understand how paternal exposure to predation risk prior to mating alters reproductive traits and parental care behaviour in unexposed F1 sons and F2 grandsons. Sons of predator-exposed fathers took more attempts to mate than sons of control fathers. F1 sons and F2 grandsons with two (maternal and paternal) predator-exposed grandfathers shifted their paternal care (fanning) behaviour in strikingly similar ways: they fanned less initially, but fanned more near egg hatching. This shift in fanning behaviour matches shifts observed in response to direct exposure to predation risk, suggesting a highly conserved response to pre-fertilization predator exposure that persists from the F0 to the F1 and F2 generations.

Offspring overcome poor parenting by being better parents.

The evolutionary repercussions of parental effects-the impact of the developmental environment provided by parents on offspring-are often discussed as static effects that can have negative influences on offspring fitness that may even persist across generations. However, individuals are not passive recipients and may mitigate the persistence of parental effects through their behaviour. Here, we tested how the burying beetle, Nicrophorus orbicollis, a species with complex parental care, responded to poor parenting. We cross-fostered young and manipulated the duration of parental care received and measured the impact on traits of both F1 and F2 offspring to experimentally extricate the effect of poor parenting from other parental effects. As expected, reducing parental care negatively affected traits that are ecologically important for burying beetles, including F1 offspring development time and body size. However, F1 parents that received reduced care as larvae spent more time feeding F2 offspring than parents that received full care as larvae. As a result, both the number and mass of F2 offspring were unaffected by the developmental experience of their parents. Our results show that flexible parental care may be able to overcome poor developmental environments and limit negative parental effects to a single generation.

Advancing Maternal Transfer of Organic Pollutants across Reptiles for Conservation and Risk Assessment Purposes.

Embryonic exposure through maternally transferred pollutants can affect embryo vitality, survival, and health. Reptiles face global declines and are sensitive to embryonic pollutant exposure. Yet, they are often neglected in pollution risk assessment and conservation. We analyzed maternal transfer of organic pollutants in reptiles through a systematic extraction, homogenization, and integration of published data on organic pollutants measured in mother-egg pairs into a comprehensive database (DOI:10.5281/zenodo.10900226), complemented with molecular physical-chemical properties of the pollutants. Over four decades, 17 publications provided 19,955 data points shifting from legacy to emerging contaminants although research on newer contaminants lags regulatory and societal demands. Challenges including taxonomic bias, heterogeneity in sampled tissues, and 73% of censored data complicate comparative analyses. However, significant opportunities were identified including the use of the turtle Malachlemys terrapin and snake Enhydris chinensis as flagship species where a large amount of data is available across tissues (allowing investigation into physiological relations) and compounds (allowing insights into maternal transfer across the chemical universe). Data on other freshwater and marine turtles provide the possibility of exploring taxonomic patterns in this subgroup. The analysis, integrated database, and discussion present opportunities for research in an era where science needs to achieve more with limited wildlife data.

Maternal effects, paternal effects, and their interactions in the freshwater snail Physa acuta.

Individuals exposed to predation risk can produce offspring with altered phenotypes. Most work on predation-induced parental effects has focused on maternal effects or on generalized parental effects where both parents are exposed to risk. We conducted an experiment to measure and compare maternal and paternal effects on offspring phenotypes and test for interactions in those effects. We exposed 82 snails from 22 lines to control or predator cues and created line dyads with the four possible mating pairings of control and predator cue exposed individuals. We measured the resulting body masses, shell masses, shell shapes, and anti-predator behaviors of the offspring. We found some evidence that offspring were larger and heavier when the mother was exposed to predation cues, but that this effect was negated when the father was also exposed. The mass of offspring shells relative to their total mass was unaffected by parental treatments. Shell shape was marginally affected by maternal treatment, but not paternal treatment. Behavioral responses to cues were not affected by maternal or paternal treatments. Our results suggest potential conflict between male and female parental effects and highlight the importance of examining the interactions of maternal and paternal effects.

Kangaroo Fathers Modulate Maternal Control of Offspring Sex but Not Postpartum Maternal Expenditure.

AbstractWhen sons and daughters have different fitness costs and benefits, selection may favor deviations from an even offspring sex ratio. Most theories on sex ratio manipulation focus on maternal strategies and sex-biased maternal expenditure. Recent studies report paternal influences on both offspring sex ratio and postpartum sex-biased maternal expenditure. We used long-term data on marked kangaroos to investigate whether and how paternal mass and skeletal size, both determinants of male reproductive success, influenced (a) offspring sex in interaction with maternal mass and (b) postpartum sex-biased maternal expenditure. When mothers were light, the probability of having a son increased with paternal mass. Heavy mothers showed the opposite trend. A similar result emerged when considering paternal size instead of mass. Postpartum maternal sex-specific expenditure was independent of paternal mass or size. Studies of offspring sex manipulation or maternal expenditure would benefit from an explicit consideration of paternal traits, as paternal and maternal effects can modulate each other.

Maternal and Paternal Age Effects on Male Antler Flies: A Field Experiment.

AbstractIn many species, parental age at reproduction can influence offspring performance and life span, but the direction of these effects and the traits affected vary among studies. Data on parental age effects are still scarce in noncaptive populations, especially insects, despite species such as fruit flies being models in laboratory-based aging research. We performed a biologically relevant experimental manipulation of maternal and paternal age at reproduction of antler flies (Protopiophila litigata) in the laboratory and tracked the adult life span and reproductive success of their male offspring released in the wild. Increased paternal, but not maternal, age somewhat increased sons' adult life span, while parental ages did not influence sons' mating rate or reproductive senescence. Our results indicate that while parental age effects do exist in an insect in the field, they may be beneficial in such a short-lived animal, in contrast to results from most wild vertebrates and laboratory invertebrates.

Intermediate confounding in trio relationships: The importance of complete data in effect size estimation.

We present an important characteristic of trio models which may lead to bias and loss of power when one parent is unmodeled in trio analyses. Motivated by recent interest in estimating parental effects on postnatal and later-life phenotypes, we consider a causal model where each parent has both an effect on their child's phenotype which is mediated through the genotype transmitted to the child and a direct effect on the phenotype through the parentally provided environment. We derive the power and bias of models in which one parent's genotype is not modeled, showing that while the effect of the child's genotype is biased in the direction of the unmodeled parent's effect as expected, the estimated effect of the observed parent's genotype is also biased in the opposite direction. While this phenomenon may not be intuitive under the assumption of random mating, it can be explained by intermediate confounding of the child's genotype-phenotype effect. These observations have implications for the accurate estimation of maternal and paternal effects in trio data sets with missing genotype data.

Parent-specific effects on risk of developing allergic sensitization and asthma in childhood.

BACKGROUND: Parent's history of atopic traits increases the risk of the same traits in their children, but mother's history may confer an increased risk compared to father's history. OBJECTIVE: To investigate parent-specific effects on risk of developing allergic sensitization and asthma in childhood. METHODS: We included 685 parent-child trios from the Copenhagen Prospective Studies on Asthma in Childhood 2010 (COPSAC2010) cohort. Parent's asthma was assessed by structured interviews and child's asthma was diagnosed prospectively at regular visits to the COPSAC clinic until age 6. Specific IgE and total IgE levels were measured in parents and children by age 0.5, 1.5 and 6 years. Associations between parent and child disease traits were analyzed using general estimating equations model adjusted for breastfeeding and maternal smoking during 3rd trimester. RESULTS: Maternal compared to paternal elevated specific IgE increased the child's risk of elevated specific IgE from 0-6 years: adjusted odds ratio (aOR)mother = 1.49 [1.09-2.03], P = .01 and aORfather = 1.32 [0.96-1.82], P = .08. Maternal elevated total IgE also increased the child's risk of elevated total IgE: adjusted relative risk (aOR)mother = 4.32 [1.51-10.8], P < .01, while a trend was observed for paternal total IgE: aORfather = 2.01 [0.76-4.82], P = .13. Individual time point analyses showed that the maternal effect was strongest in early life, whereas the parental effects were comparable by age 6. A similar parent-specific pattern was observed for the child's risk of asthma. CONCLUSIONS AND CLINICAL RELEVANCE: The effect of mother's history of atopic traits on the child's risk of developing the same traits in early childhood was stronger than the effect from father's history, which was not evident before age 6. This suggests that maternal non-genetic factors seem to confer an added disease risk to the child, particularly in early life.

Offspring phenotype is shaped by the nonsperm fraction of semen.

In a large majority of animal species, the only contribution of males to the next generation has been assumed to be their genes (sperm). However, along with sperm, seminal plasma contains a wide array of extracellular factors that have many important functions in reproduction. Yet, the potential intergenerational effects of these factors are virtually unknown. We investigated these effects in European whitefish (Coregonus lavaretus) by experimentally manipulating the presence and identity of seminal plasma and by fertilizing the eggs of multiple females with the manipulated and unmanipulated semen of several males in a full-factorial breeding design. The presence of both own seminal plasma and foreign seminal plasma inhibited sperm motility, and the removal of own seminal plasma decreased embryo survival. Embryos hatched significantly earlier after both semen manipulations than in control fertilizations; foreign seminal plasma also increased offspring aerobic swimming performance. Given that our experimental design allowed us to control potentially confounding sperm-mediated (sire) effects and maternal effects, our results indicate that seminal plasma may have direct intergenerational consequences for offspring phenotype and performance. This novel source of offspring phenotypic variance may provide new insights into the evolution of polyandry and mechanisms that maintain heritable variation in fitness and associated female mating preferences.

Intergenerational effects of paternal predator cue exposure on behavior, stress reactivity, and neural gene expression.

Predation threat impacts prey behavior, physiology, and fitness. Stress-mediated alterations to the paternal epigenome can be transmitted to offspring via the germline, conferring a potential advantage to offspring in predator-rich environments. While intergenerational epigenetic transmission of paternal experience has been demonstrated in mammals, how paternal predator exposure might alter offspring phenotypes across development is unstudied. We exposed male mice to a predator odor (2,4,5-trimethylthiazoline, TMT) or a neutral odor (banana extract) prior to mating and measured offspring behavioral phenotypes throughout development, together with adult stress reactivity and candidate gene expression in the prefrontal cortex, hippocampus, amygdala, and hypothalamus. We predicted that offspring of TMT-exposed males would be less active, would display elevated anxiety-like behaviors, and would have a more efficient stress response relative to controls, phenotypes that should enhance predator avoidance in a high predation risk environment. Unexpectedly, we found that offspring of TMT-exposed males are more active, exhibit less anxiety-like behavior, and have decreased baseline plasma corticosterone relative to controls. Effects of paternal treatment on neural gene expression were limited to the prefrontal cortex, with increased mineralocorticoid receptor expression and a trend towards increased Bdnf expression in offspring of TMT-exposed males. These results suggest that fathers exposed to predation threat produce offspring that are buffered against non-acute stressors and, potentially, better adapted to a predator-dense environment because they avoid trade-offs between predator avoidance and foraging and reproduction. This study provides evidence that ecologically relevant paternal experience can be transmitted through the germline, and can impact offspring phenotypes throughout development.

Sex-specific plasticity across generations II: Grandpaternal effects are lineage specific and sex specific.

Transgenerational plasticity (TGP) occurs when the environment encountered by one generation (F0) alters the phenotypes of one or more future generations (e.g. F1 and F2). Sex selective TGP, via specific lineages or to only male or female descendants, has been underexplored in natural systems, and may be adaptive if it allows past generations to fine-tune the phenotypes of future generations in response to sex-specific life-history strategies. We sought to understand if exposing males to predation risk can influence grandoffspring via sperm in three-spined stickleback Gasterosteus aculeatus. We specifically tested the hypothesis that grandparental effects are transmitted in a sex-specific way down the male lineage, from paternal grandfathers to F2 males. We reared F1 offspring of unexposed and predator-exposed F0 males under 'control' conditions and used them to generate F2s with control grandfathers, a predator-exposed maternal grandfather (i.e. predator-exposed F0 males to F1 daughters to F2s), a predator-exposed paternal grandfather (i.e. predator-exposed F0 males to F1 sons to F2s) or two predator-exposed grandfathers. We then assayed male and female F2s for a variety of traits related to antipredator defence. We found little evidence that transgenerational effects were mediated to only male descendants via the paternal lineage. Instead, grandpaternal effects depended on lineage and were mediated largely across sexes, from F1 males to F2 females and from F1 females to F2 males. When their paternal grandfather was exposed to predation risk, female F2s were heavier and showed a reduced change in behaviour in response to a simulated predator attack relative to grandoffspring of control, unexposed grandparents. In contrast, male F2s showed reduced antipredator behaviour when their maternal grandfather was exposed to predation risk. However, these patterns were only evident when one grandfather, but not both grandfathers, was exposed to predation risk, suggesting the potential for non-additive interactions across lineages. If sex-specific and lineage effects are common, then grandparental effects are likely underestimated in the literature. These results draw attention to the importance of sex-selective inheritance of environmental effects and raise new questions about the proximate and ultimate causes of selective transmission across generations.

Early life of fathers affects offspring fitness in a wild rodent.

Intergenerational fitness effects on offspring due to the early life of the parent are well studied from the standpoint of the maternal environment, but intergenerational effects owing to the paternal early life environment are often overlooked. Nonetheless, recent laboratory studies in mammals and ecologically relevant studies in invertebrates predict that paternal effects can have a major impact on the offspring's phenotype. These nongenetic, environment-dependent paternal effects provide a mechanism for fathers to transmit environmental information to their offspring and could allow rapid adaptation. We used the bank vole Myodes glareolus, a wild rodent species with no paternal care, to test the hypothesis that a high population density environment in the early life of fathers can affect traits associated with offspring fitness. We show that the protein content in the diet and/or social environment experienced during the father's early life (prenatal and weaning) influence the phenotype and survival of his offspring and may indicate adaptation to density-dependent costs. Furthermore, we show that experiencing multiple environmental factors during the paternal early life can lead to a different outcome on the offspring phenotype than stimulated by experience of a single environmental factor, highlighting the need to study developmental experiences in tandem rather than independent of each other.

Maternal reproductive senescence shapes the fitness consequences of the parental age difference in ruffed lemurs.

In humans, pronounced age differences between parents have deleterious fitness consequences. In particular, the number of children is lower when mothers are much older than fathers. However, previous analyses failed to disentangle the influence of differential parental age per se from a direct age effect of each parent. In this study, we analyse the fitness consequences of both parental age and parental age differences on litter size and offspring survival in two closely related species of lemurs living in captivity. As captive lemurs do not choose their reproductive partner, we were able to measure litter size and offspring survival across breeding pairs showing a wide range of parental age differences. However, we demonstrated that the effect of the parental age difference on litter size was fully accounted for by female reproductive senescence because females mating with much younger males were old females. On the other hand, both parental age difference and female reproductive senescence influenced offspring survival. Our results emphasize the importance of teasing apart the effect of parental reproductive senescence when investigating the health and fitness consequences of parental age differences and also provide new insights for conservation programmes of endangered species.

Sperm pre-fertilization thermal environment shapes offspring phenotype and performance.

The sperm pre-fertilization environment has recently been suggested to mediate remarkable transgenerational consequences for offspring phenotype (transgenerational plasticity, TGB), but the adaptive significance of the process has remained unclear. Here, we studied the transgenerational effects of sperm pre-fertilization thermal environment in a cold-adapted salmonid, the European whitefish (Coregonus lavaretus). We used a full-factorial breeding design where the eggs of five females were fertilized with the milt of 10 males that had been pre-incubated at two different temperatures (3.5°C and 6.5°C) for 15 h prior to fertilization. Thermal manipulation did not affect sperm motility, cell size, fertilization success or embryo mortality. However, offspring that were fertilized with 6.5°C-exposed milt were smaller and had poorer swimming performance than their full-siblings that had been fertilized with the 3.5°C-exposed milt. Furthermore, the effect of milt treatment on embryo mortality varied among different females (treatment×female interaction) and male-female combinations (treatment×female×male interaction). Together, these results indicate that sperm pre-fertilization thermal environment shapes offspring phenotype and post-hatching performance and modifies both the magnitude of female (dam) effects and the compatibility of the gametes. Generally, our results suggest that short-term changes in sperm thermal conditions may have negative impact for offspring fitness. Thus, sperm thermal environment may have an important role in determining the adaptation potential of organisms to climate change. Detailed mechanism(s) behind our findings require further attention.

Differential Allocation Revisited: When Should Mate Quality Affect Parental Investment?

Differential allocation (DA) is the adaptive adjustment of reproductive investment (up or down) according to partner quality. A lack of theoretical treatments has led to some confusion in the interpretation of DA in the empirical literature. We present a formal framework for DA that highlights the nature of reproductive benefits versus costs for females mated to males of different quality. Contrary to popular belief, analytical and stochastic dynamic models both show that additive benefits of male quality on offspring fitness have no effect on optimal levels of female investment and thus cannot produce DA. Instead, if offspring fitness is affected multiplicatively by male quality, or male quality affects the female cost function, DA is expected because of changes in the marginal benefits or costs of extra investment. Additive male quality effects on the female cost function can cause a novel form of weak DA, because reduced costs can slightly favor current over future reproduction. Combinations of these distinct effects in more realistic model scenarios can explain various patterns of positive and negative DA reported for different species and mating systems. Our model therefore sheds new light on the diversity of empirical results by providing a strong conceptual framework for the DA hypothesis.

Does stronger pollen competition improve offspring fitness when pollen load does not vary?

PREMISE OF THE STUDY: Competition among pollen grains from a single donor is expected to increase the quality of the offspring produced because of the recessive deleterious alleles expressed during pollen-tube growth. However, evidence for such an effect is inconclusive; a large number of studies suffer from confounding variation in pollen competition with variation in pollen load. METHODS: In this study, we tested the effect of pollen competition on offspring performance independently of pollen-load variation. We compared seed mass and early seedling performance in Dalechampia scandens (Euphorbiaceae) between crosses in which variation in pollen competition was achieved, without variation in pollen load, by manipulating the dispersion of pollen grains on the stigmas. KEY RESULTS: Despite a large sample size (211 crosses on 20 maternal plants), we failed to find an effect of pollen competition on seed characteristics or early seedling performance. Paternal effects were always limited, and pollen competition never reduced the within-father (residual) variance. CONCLUSION: These results suggest that limited within-donor variation in genetic quality of pollen grains reduces the potential benefits of pollen competition in the study population. The lack of paternal effects on early sporophyte performance further suggests that benefits of pollen competition among pollen from multiple donors should be limited as well, and it raises questions about the significance of pollen competition as a mechanism of sexual selection.

Paternal epigenetic effects of population density on locust phase-related characteristics associated with heat-shock protein expression.

Many species exhibit transgenerational plasticity by which environmental cues experienced by either parent can be transmitted to their offspring, resulting in phenotypic variants in offspring to match ancestral environments. However, the manner by which paternal experiences affect offspring plasticity through epigenetic inheritance in animals generally remains unclear. In this study, we examined the transgenerational effects of population density on phase-related traits in the migratory locust Locusta migratoria. Using an experimental design that explicitly controls genetic background, we found that the effects of crowd or isolation rearing on phase plasticity could be inherited to the offspring. The isolation of gregarious locusts resulted in reduced weight in offspring eggs and altered morphometric traits in hatchlings, whereas crowding of solitarious locusts exhibited opposite effects. The consequences of density changes were transmitted by both maternal and paternal inheritance, although the expression of paternal effects was not as pronounced as that of maternal effects. Prominent expression of heat-shock proteins (Hsps), such as Hsp90, Hsp70 and Hsp20.6, could be triggered by density changes. Hsps were significantly upregulated upon crowding but downregulated upon isolation. The variation in parental Hsp expression was also transmitted to the offspring, in which the pattern of inheritance was consistent with that of phase characteristics. These results revealed a paternal effect on phase polyphenism and Hsp expression induced by population density, and defined a model system that could be used to study the paternal epigenetic inheritance of environmental changes.

Inheritance of photoperiodic control of larval diapause in the Asian corn borer Ostrinia furnacalis (Guenée).

The Asian corn borer, Ostrinia furnacalis enters diapause as fully grown larvae. Owing to geographical variation in photoperiodic control of diapause, the subtropical strain from Hefei city (HF) enters diapause in response to short daylengths, whereas the tropical strain from Ledong county (LD) exhibits almost no diapause under the same conditions. The two strains were used in crosses to study the inheritance of diapause. The HF strain showed a typical long-day response with a critical daylength of approximately 14.97 h at 22 °C, 14.60 h at 25 °C and 13.68 h at 28 °C. The LD strain showed weak photoperiodic responses at 22 and 25 °C; and the F1 progeny also showed a long-day response with significantly shorter critical daylength compared with the HF strain. However, the LD × HF (F × M) crosses had significantly longer critical daylengths than HF × LD crosses, indicating a sexual bias in the inheritance of diapause induction, with the male parent having more influence on the F1 progeny. The critical daylength in a backcross to HF was significantly longer than a backcross to LD. Whether the inheritance of diapause fits an additive hypothesis or not depended on photoperiod, with results from different photoperiods showing additive inheritance or incomplete dominance of either diapause or non-diapause. Unlike diapause induction, the duration of diapause for reciprocal crosses was equally influenced by each parent, suggesting that diapause incidence and maintenance are controlled by separate systems in O. furnacalis.

The impact of paternal factors on cleavage stage and blastocyst development analyzed by time-lapse imaging-a retrospective observational study.

PURPOSE: Various time-lapse studies have postulated embryo selection criteria based on early morphokinetic markers. However, late paternal effects are mostly not visible before embryonic genome activation. The primary objective of this retrospective study was to investigate whether those early morphokinetic algorithms investigated by time-lapse imaging are reliable enough to allow for the accurate selection of those embryos that develop into blastocysts, while of course taking into account the correlation with the type of injected spermatozoa. METHODS: During a period of 18 months, a total of 461 MII oocytes from 43 couples with severe male factor infertility and previous "external" IVF failures after cleavage-stage embryo transfer (ET) were fertilized by intracytoplasmic morphologically selected sperm injection (IMSI). Thereof, 373 embryos were monitored in a time-lapse incubator until ET on day 5. Blastocyst outcome in combination with three previously postulated MKc (cc2: t3-t2, 5-12 h; t3, 35-40 h; t5, 48-56 h) and the morphology of the selected sperm were analyzed. RESULTS: A significant increase in the rate of blastocysts (54.0 vs. 36.3 %; P < 0.01) and top blastocysts (25.3 vs. 10.8 %; P < 0.001) was observed in the group of those meeting all three morphokinetic criteria (MKc3). However, MKc3 were only met in 23.3 % of all embryos. Moreover, TBR was influenced by the type of injected spermatozoa. In both groups, TBR decreased dramatically (MKc3, 35.0 vs. 17.0 %; MKc < 3, 14.2 vs. 8.4 %) when class II/III sperm instead of class I were injected. CONCLUSION: Early morphokinetic parameters might give some predictive information but fail to serve as a feasible selective tool for the prediction of blastocyst development given the influence of the type of spermatozoa injected.

Revisiting telegony: offspring inherit an acquired characteristic of their mother's previous mate.

Newly discovered non-genetic mechanisms break the link between genes and inheritance, thereby also raising the possibility that previous mating partners could influence traits in offspring sired by subsequent males that mate with the same female ('telegony'). In the fly Telostylinus angusticollis, males transmit their environmentally acquired condition via paternal effects on offspring body size. We manipulated male condition, and mated females to two males in high or low condition in a fully crossed design. Although the second male sired a large majority of offspring, offspring body size was influenced by the condition of the first male. This effect was not observed when females were exposed to the first male without mating, implicating semen-mediated effects rather than female differential allocation based on pre-mating assessment of male quality. Our results reveal a novel type of transgenerational effect with potential implications for the evolution of reproductive strategies.