The effect of maternal and paternal environments on seed characters in the herbaceous plant Campanula Americana (Campanulaceae)

Maternal environments typically influence the phenotype of their offspring. However, the effect of the paternal environment or the potential for joint effects of both parental environments on offspring characters is poorly understood. Two populations of Campanula americana, a woodland herb with a variable life history, were used to determine the influence of maternal and paternal light and nutrient environments on offspring seed characters. Families were grown in the greenhouse in three levels of light or three levels of nutrients. Crosses were conducted within each environmental gradient to produce seeds with all combinations of maternal and paternal environments. On average, increasing maternal nutrient and light levels increased seed mass and decreased percentage germination. The paternal environment affected seed mass, germination time, and percentage germination. However, the influence of the paternal environment varied across maternal environments, suggesting that paternal environmental effects should be evaluated in the context of maternal environments. Significant interactions between family and the parental environments for offspring characters suggest that parental environmental effects are genetically variable. In C. americana, the timing of germination determines life history. Therefore parental environmental effects on germination timing, and genetic variation in those parental effects, suggest that parental environments may influence life history evolution in this system.     

Testing population differentiation in plant species – how important are environmental maternal effects

The maternal environment may contribute to population differentiation in offspring traits if growing conditions of mother plants are different. However, the magnitude of such environmental maternal effects compared with genetic differentiation is often not clear. We tested the importance of environmental maternal effects by comparing population differentiation in parental seed directly collected in the field and in F₁ seed grown under homogeneous conditions. The F₁ seeds were obtained by random crosses within populations. We used five populations in each of four plant species to analyse seed mass and growth chamber germination of both generations at the same time. In two species, we additionally tested offspring performance in the field. We found a significant population differentiation in all species and for nearly all measured traits. Population‐by‐generation interactions indicating environmental maternal effects were significant for germination (three species) and for seed mass (two species) but not for growth and reproduction. The significant interaction was partly due to a reduction of among‐population differentiation from the parental to the F₁ generation that can be explained by a decrease of maternal provisioning effects. However, in some species by trait combinations a change in population ranking and not a decrease of variation was responsible for significant population‐by‐generation interactions indicating environmental maternal effects beyond maternal provisioning. Fitting of seed mass as covariate was not successful in reducing environmental maternal effects on population differentiation in germination. We discuss alternative methods to account for environmental maternal effects in studies on genetic differentiation among populations.     

EFFECTS OF MATERNAL AND PATERNAL ENVIRONMENT AND GENOTYPE ON OFFSPRING PHENOTYPE IN SOLIDAGO ALTISSIMA L.

To predict the possible evolutionary response of a plant species to a new environment, it is necessary to separate genetic from environmental sources of phenotypic variation. In a case study of the invader Solidago altissima, the influences of several kinds of parental effects and of direct inheritance and environment on offspring phenotype were separated. Fifteen genotypes were crossed in three 5 × 5 diallels excluding selfs. Clonal replicates of the parental genotypes were grown in two environments such that each diallel could be made with maternal/paternal plants from sand/sand, sand/soil, soil/sand, and soil/soil. In a first experiment (1989) offspring were raised in the experimental garden and in a second experiment (1990) in the glasshouse. Parent plants growing in sand invested less biomass in inflorescences but produced larger seeds than parent plants growing in soil. In the garden experiment, phenotypic variation among offspring was greatly influenced by environmental heterogeneity. Direct genetic variation (within diallels) was found only for leaf characters and total leaf mass. Germination probability and early seedling mass were significantly affected by phenotypic differences among maternal plants because of genotype ( genetic maternal effects ) and soil environment ( general environmental maternal effects ). Seeds from maternal plants in sand germinated better and produced bigger seedlings than seeds from maternal plants in soil. They also grew taller with time, probably because competition accentuated the initial differences. Height growth and stem mass at harvest (an integrated account of individual growth history) of offspring varied significantly among crosses within parental combinations ( specific environmental maternal effects ). In the glasshouse experiment, the influence of environmental heterogeneity and competition could be kept low. Except for early characters, the influence of direct genetic variation was large but again leaf characters (= basic module morphology) seemed to be under stricter genetic control than did size characters. Genetic maternal effects, general environmental maternal effects, and specific environmental maternal effects dominated in early characters. The maternal effects were exerted both via seed mass and directly on characters of young offspring. Persistent effects of the general paternal environment ( general environmental paternal effects ) were found for leaf length and stem and leaf mass at harvest. They were opposite in direction to the general environmental maternal effects, that is the same genotypes produced “better mothers” in sand but “better fathers” in soil. The general environmental paternal effects must have been due to differences in pollen quality, resulting from pollen selection within the male parent or leading to pre- or postzygotic selection within the female parent. The ranking of crosses according to mean offspring phenotypes was different in the two experiments, suggesting strong interaction of the observed effects with the environment. The correlation structure among characters changed less between experiments than did the pattern of variation of single characters, but under the competitive conditions in the garden plant height seemed to be more directly related to fitness than in the glasshouse. Reduced competition could also explain why maternal effects were less persistent in the glasshouse than in the garden experiment. Evolution via selection of maternal effects would be possible in the study population because these effects are in part due to genetic differences among parents.     

Variation among populations of Diodia teres (Rubiaceae) in environmental maternal effects

Previous studies have quantified variation in environmental maternal effects (EME) within populations, but these effects could differ among populations as well. In this study we grew clonal replicates of individuals from three populations of the annual plant Diodia teres in their native and non-native environments. Our goal was to estimate the effects of maternal environment and maternal population on seed and seedling traits. Seeds that were produced in this field study were then planted in two soil types to quantify effects of the offspring environment on seedling traits. There was substantial variation among populations for seed weight. We found population variation for EME, and maternal environment by offspring environment interactions. We conclude that variation among populations in EME may be an unrecognized component of local adaptation, and that attempts to control maternal effects by statistically accounting for variation in seed weight may be ineffective.     

Maternal environmental effects of competition influence evolutionary potential in rapeseed (<Emphasis Type="Italic">Brassica</Emphasis><Emphasis Type="Italic">rapa</Emphasis>)

Maternal environmental effects reflect the contribution of the maternal environment to the offspring phenotype. Maternal effects are prevalent in plants and animals and may undergo adaptive evolution and affect patterns of natural selection within and across generations. Here, we raise two generations of a rapeseed (Brassica rapa) population derived from a cross between a rapid-cycling and an oilseed genotype in competitive and noncompetitive settings. Maternal environment had little effect on average offspring phenotypes. Maternal genotypes, however, differed in the sensitivity of almost all offspring phenotypes to the maternal environment, demonstrating genetic variation in maternal effects for traits expressed throughout ontogeny. Maternal environment did not significantly affect progeny seed production, and maternal genotypes were not variable for this trait, indicating no evidence for direct maternal effects on offspring fitness. Maternal environment influenced natural selection in the progeny generation; disruptive selection acted on seed mass among seeds matured in the noncompetitive maternal environment versus no significant selection on this trait for seeds matured in the competitive maternal environment. Although maternal effects did not directly increase fitness, they did affect evolutionary potential and selection in the progeny generation. These results suggest that diverse phenotypes of both wild and cultivated B. rapa genotypes will depend on the maternal environment in which the seeds are matured.     

Grandparental effects in marine sticklebacks: transgenerational plasticity across multiple generations

Nongenetic inheritance mechanisms such as transgenerational plasticity (TGP) can buffer populations against rapid environmental change such as ocean warming. Yet, little is known about how long these effects persist and whether they are cumulative over generations. Here, we tested for adaptive TGP in response to simulated ocean warming across parental and grandparental generations of marine sticklebacks. Grandparents were acclimated for two months during reproductive conditioning, whereas parents experienced developmental acclimation, allowing us to compare the fitness consequences of short‐term vs. prolonged exposure to elevated temperature across multiple generations. We found that reproductive output of F1 adults was primarily determined by maternal developmental temperature, but carry‐over effects from grandparental acclimation environments resulted in cumulative negative effects of elevated temperature on hatching success. In very early stages of growth, F2 offspring reached larger sizes in their respective paternal and grandparental environment down the paternal line, suggesting that other factors than just the paternal genome may be transferred between generations. In later growth stages, maternal and maternal granddam environments strongly influenced offspring body size, but in opposing directions, indicating that the mechanism(s) underlying the transfer of environmental information may have differed between acute and developmental acclimation experienced by the two generations. Taken together, our results suggest that the fitness consequences of parental and grandparental TGP are highly context dependent, but will play an important role in mediating some of the impacts of rapid climate change in this system.     

Maternal effects provide phenotypic adaptation to local environmental conditions

In outcrossing plants, seed dispersal distance is often less than pollen movement. If the scale of environmental heterogeneity within a population is greater than typical seed dispersal distances but less than pollen movement, an individual's environment will be similar to that of its mother but not necessarily its father. Under these conditions, environmental maternal effects may evolve as a source of adaptive plasticity between generations, enhancing offspring fitness in the environment that they are likely to experience. This idea is illustrated using Campanula americana, an herb that grows in understory and light-gap habitats. Estimates of seed dispersal suggest that offspring typically experience the same light environment as their mother. In a field experiment testing the effect of open vs understory maternal light environments, maternal light directly influenced offspring germination rate and season, and indirectly affected germination season by altering maternal flowering time. Results to date indicate that these maternal effects are adaptive; further experimental tests are ongoing. Evaluating maternal environmental effects in an ecological context demonstrates that they may provide phenotypic adaptation to local environmental conditions.     

The thrifty phenotype as an adaptive maternal effect

Human diseases in adulthood are increasingly associated with growth patterns in early life, implicating early-life nutrition as the underlying mechanism. The thrifty phenotype hypothesis proposed that early-life metabolic adaptations promote survival, with the developing organism responding to cues of environmental quality by selecting an appropriate trajectory of growth. Recently, some authors have proposed that the thrifty phenotype is also adaptive in the longer-term, by preparing the organism for its likely adult environment. However, windows of plasticity close early during human development, and subsequent environmental changes may result in the selected trajectory becoming inappropriate, leading to adverse effects on health. This paradox generates uncertainty as to whether the thrifty phenotype is indeed adaptive for the offspring in humans. The thrifty phenotype should not be considered a dichotomous concept, rather it refers to the capacity of all offspring to respond to environmental information during early ontogenetic development. This article argues that the thrifty phenotype is the consequence of three different adaptive processes - niche construction, maternal effects, and developmental plasticity - all of which in humans are influenced by our large brains. While developmental plasticity represents an adaptation by the offspring, both niche construction and parental effects are subject to selection on parental rather than offspring fitness. The three processes also operate at different paces. Human offspring do not become net calories-producers until around 18 years of age, such that the high energy costs of the human brain are paid primarily by the mother, even after weaning. The evolutionary expansion of human brain volume occurred in environments characterised by high volatility, inducing strong selective pressure on maternal capacity to provision multiple offspring simultaneously. The thrifty phenotype is therefore best considered as a manipulation of offspring phenotype for the benefit of maternal fitness. The information that enters offspring phenotype during early development does not predict the likely future environment of the offspring, but rather reflects the mother's own developmental experience and the quality of the environment during her own maturation. Offspring growth trajectory thus becomes aligned with long-term maternal capacity to provision. In contemporary populations, the sensitivity of offspring development to maternal phenotype exposes the offspring to adverse effects, through four distinct pathways. The offspring may be exposed to (1) poor maternal metabolic control (e.g. gestational diabetes), (2) maternally derived toxins (e.g. maternal smoking), or (3) low maternal social status (e.g. small size). Adverse consequences of these effects may then be exacerbated by (4) exposure either to the "toxic" western environment in postnatal life, in which diet and physical activity levels are mismatched with metabolic experience in utero, or at the other extreme to famine. The rapid emergence of the epidemic of the metabolic syndrome in the 20th Century reflects the rapid acceleration in the pace of niche construction relative to the slower physiological combination of developmental plasticity and parental effects.     

Parental effects in Plantago lanceolata L. III. Measuring parental temperature effects in the field

To determine the evolutionary importance of parental environmental effects in natural populations, we must begin to measure the magnitude of these effects in the field. For this reason, we conducted a combined growth chamber-field experiment to measure parental temperature effects in Plantago lanceolata. We grew in the field offspring of controlled crosses of chamber-grown parents subjected to six temperature treatments. Each treatment was characterized by a unique combination of maternal prezygotic (prior to fertilization), paternal prezygotic, and postzygotic (during fertilization and seed set) temperatures. Offspring were followed for three years to measure the effects of treatment on several life-history traits and population growth rate, our estimate of fitness. Parental treatment influenced germination, growth, and reproduction of newborns, but not survival or reproduction of offspring at least one year old. High postzygotic temperature significantly increased germination and leaf area at 17 weeks by approximately 35% and 2%, respectively. Probability of flowering and spike production in the newborn age class showed significant parental genotype x parental treatment interactions. High postzygotic temperature increased offspring fitness by approximately 50%. The strongest contributors to fitness were germination and probability of flowering and spike production of newborns. A comparison of our data with previously collected data for chambergrown offspring shows that the influence of parental environment on offspring phenotype is weaker but still biologically meaningful in the field. The results provide evidence that parental environment influences offspring fitness in natural populations of P. lanceolata and does so by affecting the life-history traits most strongly contributing to fitness. The data suggest that from the perspective of offspring fitness, natural selection favors parents that flower later in the flowering season in the North Carolina Piedmont when it is warmer. Genotypic-specific differences in response of offspring reproductive traits to parental environment suggest that parental environmental effects can influence the rate of evolutionary change in P. lanceolata.     

Maternal environment affects the genetic basis of seed dormancy in Arabidopsis thaliana

The genetic basis of seed dormancy, a key life history trait important for adaptive evolution in plant populations, has yet been studied only using seeds produced under controlled conditions in greenhouse environments. However, dormancy is strongly affected by maternal environmental conditions, and interactions between seed genotype and maternal environment have been reported. Consequently, the genetic basis of dormancy of seeds produced under natural field conditions remains unclear. We examined the effect of maternal environment on the genetic architecture of seed dormancy using a recombinant inbred line (RIL) population derived from a cross between two locally adapted populations of Arabidopsis thaliana from Italy and Sweden. We mapped quantitative trait loci (QTL) for dormancy of seeds produced in the greenhouse and at the native field sites of the parental genotypes. The Italian genotype produced seeds with stronger dormancy at fruit maturation than did the Swedish genotype in all three environments, and the maternal field environments induced higher dormancy levels compared to the greenhouse environment in both genotypes. Across the three maternal environments, a total of nine dormancy QTL were detected, three of which were only detected among seeds matured in the field, and six of which showed significant QTL × maternal environment interactions. One QTL had a large effect on dormancy across all three environments and colocalized with the candidate gene DOG1. Our results demonstrate the importance of studying the genetic basis of putatively adaptive traits under relevant conditions.     

Environmental effects on the detection of adaptation

Detecting adaptation involves comparing the performance of populations evolving in different environments. This detection may be confounded by effects due to the environment experienced by organisms prior to the test. We tested whether such confounding effects occur, using spider-mite selection lines on two novel hosts and one ancestral host, after 15 generations of selection. Mites were either sampled directly from the selection lines or subjected to a common juvenile or to a common maternal environment, mimicking the most frequent environmental manipulations. These environments strongly affected all life-history traits. Moreover, the detection of adaptation and correlated responses on the ancestral host was inconsistent among environments in almost 20% of the cases. Indeed, we did not detect responses unambiguously for any life-history trait. This inconsistency was due to differential environmental effects on lines from different selection regimes. Therefore, the detection of adaptation requires a careful control of these environmental effects.     

Quantitative genetics of growth and development time in the burying beetle Nicrophorus pustulatus in the presence and absence of post-hatching parental care

Despite a growing interest in the evolutionary aspects of maternal effects, few studies have examined the genetic consequences of maternal effects associated with parental care. To begin to provide data on nonlaboratory or nondomestic animals, we compared the effect of presence and absence of parental care on phenotype expression of larval mass and development time at different life-history stages in the burying beetle Nicrophorus pustulatus. This beetle has facultative care; parents can feed their larvae through regurgitation of digested carrion or offspring can feed by themselves from previously prepared carrion. To investigate larval responses to these two levels of care, including estimates of additive genetic effects, maternal effects, and genotype-by-environment interactions, we used a half-sibling split-family breeding experiment-raising half of the offspring of a family in the presence of their mother and the other half without their mother present. Larvae reared with their mother present were on average heavier and developed faster, although some of the differences in development decreased or were eliminated by the adult stage. These results suggest that presence or absence of post-hatching maternal care plays an important role in phenotype expression early in life, whereas later the phenotype of the offspring is determined mainly by the genotype and/or unshared environmental effects. Our study also permitted us to examine the differences in genetic effects between the two care environments. Heritabilities, maternal/common environment effect, and most genetic correlations did not differ between the care treatments. Genetic analyses revealed substantial additive genetic effects for development time but small effects for measures of body mass. Maternal plus common environment effects were high for measures of mass but low for development time, suggesting that indirect genetic effects of maternal and/or common environment are less important for the evolution of development time than for mass. Estimates of genetic correlations revealed a trade-off between the duration of the two development stages after the offspring left the carrion. There was also a negative genetic correlation between the time spent on carrion and the mass at 72 h, when mothers usually stop feeding. The analysis of genotype-by-environment interactions indicates substantial variation among maternal families in response to care. Presence or absence of parental care may therefore contribute to the additive genetic variance through its interaction with the maternal component of the additive genetic variance. The presence of this interaction further suggests that parents may vary in care strategies, with some parents dispersing after preparation of the carrion and some parents staying with the larvae. This interaction may help maintain genetic variation in growth, development time, and parental care behavior. Additional work is needed, however, to quantify indirect genetic effects and genetic variation in parental care behavior itself.     

Adaptive transgenerational plasticity in the perennial Plantago lanceolata

Phenotypes of plants, and thus their ecology and evolution, can be affected by the environmental conditions experienced by their parents, a phenomenon called parental effects or transgenerational plasticity. However, whether such effects are just passive responses or represent a special type of adaptive plasticity remains controversial because of a lack of solid tests of their adaptive significance. Here, we investigated transgenerational effects of different nutrient environments on the productivity, carbon storage and flowering phenology of the perennial plant Plantago lanceolata, and whether these effects are influenced by seasonal variation in the maternal environment. We found that maternal environments significantly affected the offspring phenotype, and that plants consistently produced more biomass and had greater root carbohydrate storage if grown under the same environmental conditions as experienced by their mothers. The observed transgenerational effects were independent of the season in which seeds had matured. We therefore conclude that transgenerational effects on biomass and carbon storage in P. lanceolata are adaptive regardless of the season of seed maturation.     

Heritability of seed weight in Maritime pine,a relevant trait in the transmission of environmental maternal effects

Quantitative seed provisioning is an important life-history trait with strong effects on offspring phenotype and fitness. As for any other trait, heritability estimates are vital for understanding its evolutionary dynamics. However, being a trait in between two generations, estimating additive genetic variation of seed provisioning requires complex quantitative genetic approaches for distinguishing between true genetic and environmental maternal effects. Here, using Maritime pine as a long-lived plant model, we quantified additive genetic variation of cone and seed weight (SW) mean and SW within-individual variation. We used a powerful approach combining both half-sib analysis and parent–offspring regression using several common garden tests established in contrasting environments to separate G, E and G × E effects. Both cone weight and SW mean showed significant genetic variation but were also influenced by the maternal environment. Most of the large variation in SW mean was attributable to additive genetic effects (h²=0.55–0.74). SW showed no apparent G × E interaction, particularly when accounting for cone weight covariation, suggesting that the maternal genotypes actively control the SW mean irrespective of the amount of resources allocated to cones. Within-individual variation in SW was low (12%) relative to between-individual variation (88%), and showed no genetic variation but was largely affected by the maternal environment, with greater variation in the less favourable sites for pine growth. In summary, results were very consistent between the parental and the offspring common garden tests, and clearly indicated heritable genetic variation for SW mean but not for within-individual variation in SW.     

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.     

Transgenerational plasticity of inducible defences: Combined effects of grand‐parental,parental and current environments

Phenotypic plasticity can occur across generations (transgenerational plasticity) when environments experienced by the previous generations influenced offspring phenotype. The evolutionary importance of transgenerational plasticity, especially regarding within‐generational plasticity, is a currently hot topic in the plasticity framework. How long an environmental effect can persist across generations and whether multigenerational effects are cumulative are primordial—for the evolutionary significance of transgenerational plasticity—but still unresolved questions. In this study, we investigated how the grand‐parental, parental and offspring exposures to predation cues shape the predator‐induced defences of offspring in the Physa acuta snail. We expected that the offspring phenotypes result from a three‐way interaction among grand‐parental, parental and offspring environments. We exposed three generations of snails without and with predator cues according to a full factorial design and measured offspring inducible defences. We found that both grand‐parental and parental exposures to predator cues impacted offspring antipredator defences, but their effects were not cumulative and depended on the defences considered. We also highlighted that the grand‐parental environment did alter reaction norms of offspring shell thickness, demonstrating an interaction between the grand‐parental transgenerational plasticity and the within‐generational plasticity. We concluded that the effects of multigenerational exposure to predator cues resulted on complex offspring phenotypic patterns which are difficult to relate to adaptive antipredator advantages.     

Life-stage specific environments in a cichlid fish: implications for inducible maternal effects

Through environmentally induced maternal effects females may fine-tune their offspring’s phenotype to the conditions offspring will encounter after birth. If juvenile and adult ecologies differ, the conditions mothers experienced as juveniles may better predict their offspring’s environment than the adult females’ conditions. Maternal effects induced by the environment experienced by females during their early ontogeny should evolve when three ecological conditions are met: (1) Adult ecology does not predict the postnatal environmental conditions of offspring; (2) Environmental conditions for juveniles are correlated across successive generations; and (3) Juveniles occasionally settle in conditions that differ from the juvenile habitat of their mothers. By combining size-structured population counts, ecological surveys and a genetic analysis of population structure we provide evidence that all three conditions hold for Simochromis pleurospilus, a cichlid fish in which mothers adjust offspring quality to their own juvenile ecology. In particular we show (1) that the spatial niches and the habitat quality differ between juveniles and adults, and we provide genetic evidence (2) that usually fish of successive generations grow up in similar habitats, and (3) that occasional dispersal in populations with a different habitat quality is likely to occur. As adults of many species cannot predict their offspring’s environment from ambient cues, life-stage specific maternal effects are likely to be common in animals. It will therefore be necessary to incorporate parental ontogeny in the study of parental effects when juveniles and adults inhabit different environments.     

Interaction between maternal effects and temperature affects diapause occurrence in the cricket Allonemobius socius

The induction of diapause can be adaptive for egg survival during unfavorable conditions, while direct development can be advantageous under favorable conditions by allowing additional generations to exploit abundant resources. Therefore, the physiological capability of a female to respond to environmental cues indicative of habitat quality by producing eggs of the appropriate developmental phenotype should be under strong selection. Additionally, developing embryos may alter the developmental trajectory initiated by the female in response to changing environmental conditions. In this study, we used a cross-fostering approach to isolate the maternal effects of parental diapause history (not previously studied) and egg-laying temperature from the influence of the incubation environment experienced by the developing embryo on the proportion of diapause eggs produced by the striped ground cricket, Allonemobius socius. We found that an interaction between egg-incubation temperature and parental diapause history strongly affected the proportion of diapause eggs produced and the proportion of eggs that hatched within a 16–18 day incubation period, while egg-laying temperature and all other interactions did not. These novel results indicate that embryos can respond directly to the environmental conditions they experience during development, but that their ability to do so is influenced by maternal effects such as parental diapause history. The results of this study not only provide evidence, for the first time, of parental diapause history affecting diapause proportions, but also raise additional questions about the mechanism by which environmental information is transmitted from parent to offspring and how offspring are able to respond to conditions experienced during their own development.     

Effects of maternal and grandmaternal flea infestation on offspring quality and quantity in a desert rodent: evidence for parasite-mediated transgenerational phenotypic plasticity

Parasites can cause a broad range of sublethal fitness effects across a wide variety of host taxa. However, a host’s efforts to compensate for possible parasite-induced fitness effects are less well-known. Parental effects may beneficially alter the offspring phenotype if parental environments sufficiently predict the offspring environment. Parasitism is a common stressor across generations; therefore, parental infestation could reliably predict the likelihood of infestation for offspring. However, little is known about relationships between parasitism and transgenerational phenotypic plasticity. Thus, we investigated how maternal and grandmaternal infestation with fleas (Xenopsylla ramesis) affected offspring quality and quantity in a desert rodent (Meriones crassus). We used a fully-crossed design with control and infested treatments to examine litter size, pup body mass at birth, and pup mass gain before weaning for combinations of maternal and grandmaternal infestation status. No effect of treatment on litter size or pup body mass at birth was found. However, maternal and grandmaternal infestation status significantly affected pre-weaning body mass gain, a proxy for the rate of maturation, in male pups. Pups gained significantly more weight before weaning if maternal and grandmaternal infestation statuses matched, regardless of the treatment. Thus, pups whose mothers and grandmothers experienced similar risks of parasitism, either both non-parasitized or both infested, would reach sexual maturity more quickly than those pups whose mothers’ infestation status did not match that of their grandmothers. These results support the contention that parents can receive external cues such as the risk of parasitism, that prompt them to alter offspring provisioning. Therefore, parasites could be a mediator of environmentally-induced maternal effects and could affect host reproductive fitness across multiple generations.