Hidden responses to environmental variation: maternal effects reveal species niche dimensions

Species responses to fluctuating environments structure population and community dynamics in variable ecosystems. Although offspring number is commonly used to measure these responses, maternal effects on offspring quality may be an important but largely unrecognised determinant of long‐term population growth. We selected 29 species across a Mediterranean annual plant phylogeny, and grew populations of each species in wet and dry conditions to determine responses in seed number and maternal effects (seed size, seed dormancy, and seedling growth). Maternal effects were evident in over 40% of species, but only 24% responded through seed number. Despite a strong trade‐off between seed size and seed number among species, there was no consistent trade‐off within species; we observed correlations that ranged from positive to negative. Overall, species in this plant guild show a complex range of responses to environmental variation that may be underestimated when only seed number responses are considered.     

Body size-specific maternal effects on the offspring environment shape juvenile phenotypes in Atlantic salmon

Positive associations between maternal investment per offspring and maternal body size have been explained as adaptive responses by females to predictable, body size-specific maternal influences on the offspring’s environment. As a larger per-offspring investment increases maternal fitness when the quality of the offspring environment is low, optimal egg size may increase with maternal body size if larger mothers create relatively poor environments for their eggs or offspring. Here, we manipulate egg size and rearing environments (gravel size, nest depth) of Atlantic salmon (Salmo salar) in a 2 × 2 × 2 factorial experiment. We find that the incubation environment typical of large and small mothers can exert predictable effects on offspring phenotypes, but the nature of these effects provides little support to the prediction that smaller eggs are better suited to nest environments created by smaller females (and vice versa). Our data indicate that the magnitude and direction of phenotypic differences between small and large offspring vary among maternal nest environments, underscoring the point that removal of offspring from the environmental context in which they are provisioned in the wild can bias experimentally derived associations between offspring size and metrics of offspring fitness. The present study also contributes to a growing literature which suggests that the fitness consequences of egg size variation are often more pronounced during the early juvenile stage, as opposed to the egg or larval stage.     

Phenotypic differentiation is associated with gender plasticity and its responsive delay to environmental changes in Alternanthera philoxeroides--phenotypic differentiation in alligator weed

Phenotypic plasticity is common in many taxa, and it may increase an organism's fitness in heterogeneous environments. However, in some cases, the frequency of environmental changes can be faster than the ability of the individual to produce new adaptive phenotypes. The importance of such a time delay in terms of individual fitness and species adaptability has not been well studied. Here, we studied gender plasticity of Alternanthera philoxeroides to address this issue through a reciprocal transplant experiment. We observed that the genders of A. philoxeroides were plastic and reversible between monoclinous and pistillody depending on habitats, the offspring maintained the maternal genders in the first year but changed from year 2 to 5, and there was a cubic relationship between the rate of population gender changes and environmental variations. This relationship indicates that the species must overcome a threshold of environmental variations to switch its developmental path ways between the two genders. This threshold and the maternal gender stability cause a significant delay of gender changes in new environments. At the same time, they result in and maintain the two distinct habitat dependent gender phenotypes. We also observed that there was a significant and adaptive life-history differentiation between monoclinous and pistillody individuals and the gender phenotypes were developmentally linked with the life-history traits. Therefore, the gender phenotypes are adaptive. Low seed production, seed germination failure and matching phenotypes to habitats by gender plasticity indicate that the adaptive phenotypic diversity in A. philoxeroides may not be the result of ecological selection, but of gender plasticity. The delay of the adaptive gender phenotype realization in changing environments can maintain the differentiation between gender systems and their associated life-history traits, which may be an important component in evolution of novel traits and taxonomic diversity.     

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.     

Egg size plasticity corresponding to maternal food conditions in an annual fish,Ayu <Emphasis Type="Italic">Plecoglossus altivelis</Emphasis>

The classic model of Smith and Fretwell predicts that the optimal egg size will vary according to the shape of the relationship between offspring size and offspring fitness, which may vary among environments. Adaptive significance of intrapopulation egg size variation was examined using Ayu (Plecoglossus altivelis). The species has an annual and migratory life history. Fish under controlled rearing conditions become sexually mature with a trend that smaller females produced larger eggs later in the season. Observed egg size variation was explained by the maternal specific growth rate, which was composed of maternal body size and growing period. Hatchlings from larger eggs had a larger notochord length, larger yolk-sac and grew faster. Such offspring traits provide general advantages of increased larval size, which confer competitive ability for assuring early survivorship. In conclusion, egg size plasticity in Ayu suggests higher offspring fitness through enhancement of their accessibility to food.     

Maternal effects of egg size in brown trout (Salmo trutta): norms of reaction to environmental quality

The magnitude of fitness variation caused by maternal effects and, thus, the adaptive significance of maternal traits may depend on environmental quality, generating crossing reaction norms among offspring phenotypes that shape life-history evolution. By manipulating intraclutch variation in egg size and comparing siblings we examined the maternal effects of egg size on offspring performance and tested for the existence of reaction norms to environmental quality using the brown trout Salmo trutta. When sibling groups of small and large eggs were reared separately in a hatchery environment initial size differences disappeared rapidly. However, in semi-natural environments and under direct competition, juveniles from large eggs experienced growth and survival advantages over siblings from small eggs. Moreover, distinct reaction norms existed, with the differences in performance of juveniles from small and large eggs being most pronounced in the poorer growth environments. Our results provide the first direct evidence, to our knowledge, for a causal relationship between egg size and fitness-related traits in fishes, independent of potentially confounding genetic effects. Moreover, they indicate that previous studies have been biased by experimental conditions that excluded competitive asymmetries and environmental variability. The existence of reaction norms indicates a shift in optimal egg size across gradients of environmental quality that probably shapes the evolution of this trait.     

Ecological and developmental context of natural selection: maternal effects and thermally induced plasticity in the frog Bombina orientalis

Variation in fitness generated by differences in functional performance can often be traced to morphological variation among individuals within natural populations. However, morphological variation itself is strongly influenced by environmental factors (e.g., temperature) and maternal effects (e.g., variation in egg size). Understanding the full ecological context of individual variation and natural selection therefore requires an integrated view of how the interaction between the environment and development structures differences in morphology, performance, and fitness. Here we use naturally occurring environmental and maternal variation in the frog Bombina orientalis in South Korea to show that ovum size, average temperature, and variance in temperature during the early developmental period affect body sizes, shapes, locomotor performance, and ultimately the probability of an individual surviving interspecific predation in predictable but nonadditive ways. Specifically, environmental variability can significantly change the relationship between maternal investment in offspring and offspring fitness so that increased maternal investment can actually negatively affect offspring over a broad range of environments. Integrating environmental variation and developmental processes into traditional approaches of studying phenotypic variation and natural selection is likely to provide a more complete picture of the ecological context of evolutionary change.     

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.     

The cost of reproduction induced by body size at birth and breeding density

Body size at birth has implications for the quality of individuals throughout their life. Although large body size is generally considered an advantage, the relationship between body size at birth and long-term fitness is often complicated. Under spatial or temporal variation in environmental conditions, such as the seasonally changing densities of Fennoscandian vole populations, selection should favor variation in offspring phenotypes, as different qualities may be beneficial in different conditions. We performed an experiment in which a novel hormonal manipulation method was used to increase phenotypic variance in body size at birth in the bank vole (Myodes glareolus). The effects of body size on the future fitness of young males and females were then studied at varying population densities in outdoor enclosures. Our results show that small body size at birth and high breeding density increase the survival costs of reproduction. However, there was no interaction between the effects of body size and density on survival, which suggests that the fitness effects of body size were strong enough to persist under environmental variation. Moreover, litter size and the probability of breeding were more sensitive to variation in breeding density than offspring size. Therefore, it is unlikely that individual fitness could be optimized by adjusting offspring body size to the prevailing population density through adaptive maternal effects. Our results highlight the significance of the costs of reproduction in the evolution of life-history traits, and give strong experimental support for the long-term fitness effects of body size at birth.     

High Altitude Frogs (Rana kukonoris) Adopt a Diversified Bethedging Strategy in the Face of Environmental Unpredictability

Environmental unpredictability can influence strategies of maternal investment among eggs within a clutch. Models predict that breeding females should adopt a diversified bet-hedging strategy in unpredictable environments, but empirical field evidence from Asia is scarce. Here we tested this hypothesis by exploring spatial patterns in egg size along an altitudinal gradient in a frog species(Rana kukunoris) inhabiting the Tibetan Plateau. Within-clutch variability in egg size increased as the environment became variable(e.g., lower mean monthly temperature and mean monthly rainfall at higher altitudes), and populations in environments with more unpredictable rainfall produced eggs that were smaller and more variable in size. We provide support for a diversified bet-hedging strategy in high-altitude environments, which experience dynamic weather patterns and therefore are of unpredictable environmental quality. This strategy may be an adaptive response to lower environmental quality and higher unpredictable environmental variance. Such a strategy should increase the likelihood of breeding success and maximize maternal lifetime fitness by producing offspring that are adapted to current environmental conditions. We speculate that in high-altitude environments prone to physical disturbance, breeding females are unable to consistently produce the optimal egg size due to physiological constraints imposed by environmental conditions(e.g., duration of the active season, food availability). Species and populations whose breeding strategies are adapted to cope with uncertain environmental conditions by adjusting offspring size and therefore quality show a remarkable degree of ability to cope with future climatic changes.     

Maternal influences on offspring phenotypes and sex ratios in a multi‐clutching lizard with environmental sex determination

Maternal and environmental factors are important sources of phenotypic variation because both factors influence offspring traits in ways that impact offspring and maternal fitness. The present study explored the effects of maternal factors (maternal body size, egg size, yolk‐steroid allocation, and oviposition‐site choice) and seasonally‐variable environmental factors on offspring phenotypes and sex ratios in a multi‐clutching lizard with environmental sex determination (Amphibolurus muricatus). Maternal identity had strong effects on offspring morphology, but the nature of maternal effects differed among successive clutches produced by females throughout the reproductive season (i.e. maternal identity by environment interactions). The among‐female and among‐clutch variation in offspring traits (including sex ratios) was not mediated through maternal body size, egg size, or variation in yolk steroid hormones. This lack of nongenetic maternal effects suggests that phenotypic variation may be generated by gene by environment interactions. These results demonstrate a significant genetic component to variation in offspring phenotypes, including sex ratios, even in species with environmental sex determination. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 256–266.     

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.     

Spatial variation in egg size and egg number reflects trade-offs and bet-hedging in a freshwater fish

1.?Maternal reproductive investment is thought to reflect a trade-off between offspring size and fecundity, and models generally predict that mothers inhabiting adverse environments will produce fewer, larger offspring. More recently, the importance of environmental unpredictability in influencing maternal investment has been considered, with some models predicting that mothers should adopt a diversified bet-hedging strategy whilst others a conservative bet-hedging strategy. 2.?We explore spatial egg size and fecundity patterns in the freshwater fish southern pygmy perch (Nannoperca australis) that inhabits a diversity of streams along gradients of environmental quality, variability and predictability. 3.?Contrary to some predictions, N.?australis populations inhabiting increasingly harsh streams produced more numerous and smaller eggs. Furthermore, within-female egg size variability increased as environments became more unpredictable. 4.?We argue that in harsh environments or those prone to physical disturbance, sources of mortality are size independent with offspring size having only a minor influence on offspring fitness. Instead, maternal fitness is maximized by producing many small eggs, increasing the likelihood that some offspring will disperse to permanent water. We also provide empirical support for diversified bet-hedging as an adaptive strategy when future environmental quality is uncertain and suggest egg size may be a more appropriate fitness measure in stable environments characterized by size-dependent fitness. These results likely reflect spatial patterns of adaptive plasticity and bet-hedging in response to both predictable and unpredictable environmental variance and highlight the importance of considering both trait averages and variance. 5.?Reproductive life-history traits can vary predictably along environmental gradients. Human activity, such as the hydrological modification of natural flow regimes, alters the form and magnitude of these gradients, and this can have both ecological and evolutionary implications for biota adapted to now non-existent natural environmental heterogeneity.     

Why does a grasshopper have fewer,larger offspring at its range limits?

Analysis of size of offspring reared through three laboratory generations from populations of the field grasshopper Chorthippus brunneus from 27 sites around the British Isles showed that offspring were larger towards the cooler-wetter conditions in the western and northern limits of the range. This variation had a significant genetic component. There was a trade-off between clutch size and offspring size between and within populations. Under favourable thermal and feeding conditions maternal fitness was optimal when individuals produced the largest clutches of the smallest eggs, but under poor conditions maternal fitness was optimal when individuals produced small clutches of very large offspring. Calculation of geometric mean fitness over time indicated that having larger offspring near to the edge of the range could be advantageous as a conservative risk-spreading strategy. As well as geographic variation in egg size, significant environment-genotype interactions in egg size in relation to temperature were observed.     

Maternal Size and Age Shape Offspring Size in a Live-Bearing Fish,Xiphophorus birchmanni

Many studies of offspring size focus on differences in maternal investment that arise from ecological factors such as predation or competition. Classic theory predicts that these ecological factors will select for an optimal offspring size, and therefore that variation in a given environment will be minimized. Yet recent evidence suggests maternal traits such as size or age could also drive meaningful variation in offspring size. The generality of this pattern is unclear, as some studies suggest that it may represent non-adaptive variation or be an artifact of temporal or spatial differences in maternal environments. To clarify this pattern, we asked how maternal size, age and condition are related to each other in several populations of the swordtail Xiphophorus birchmanni. We then determined how these traits are related to offspring size, and whether they could resolve unexplained intra-population variation in this trait. We found that female size, age, and condition are correlated within populations; at some of these sites, older, larger females produce larger offspring than do younger females. The pattern was robust to differences among most, but not all, sites. Our results document a pattern that is consistent with recent theory predicting adaptive age- and size-dependence in maternal investment. Further work is needed to rule out non-adaptive explanations for this variation. Our results suggest that female size and age could play an under-appreciated role in population growth and evolution.     

COMPETITION PROLONGS EXPRESSION OF MATERNAL EFFECTS IN SEEDLINGS OF ERIGERON ANNUUS (ASTERACEAE)

The timing of expression of environmental maternal effects on seedling growth was investigated in greenhouse-grown populations of Erigeron annuus (Asteraceae). Maternal differences were generated in genetically identical lines grown under high and low nutrient conditions. There were significant differences among maternal families within genotypes for seed size, cotyledon size, number of leaves, and rosette diameter. When seedlings were grown individually, effects of the maternal fertilizer treatment on leaf number and rosette diameter were present early but could not be detected after eight weeks. When seedlings from HIGH and LOW lines were grown in competition, the maternal effects and the relative size advantage of seedlings from HIGH parents increased throughout the experiment. Most of the variation among nutrient treatments for seedling size characters could be explained by variation in initial seed size. In the competition experiment, the increasing magnitude of maternal environmental differences over time masked genetic variation for seedling characters; without competition, the relative contribution of genetic variation increased through time. Under competitive conditions that generate persistent maternal effects on fitness, maternal environmental effects may retard natural selection.     

Phenotypic and transgenerational plasticity promote local adaptation to sun and shade environments

Adaptive plasticity is expected to be important when the grain of environmental variation is encompassed in offspring dispersal distance. We investigated patterns of local adaptation, selection and plasticity in an association of plant morphology with fine-scale habitat shifts from oak canopy understory to adjacent grassland habitat in Claytonia perfoliata. Populations from beneath the canopy of oak trees were >90 % broad leaved and large seeded, while plants from adjacent grassland habitat were >90 % linear-leaved and small seeded. In a 2-year study, we used reciprocal transplants and phenotypic selection analysis to investigate local adaptation, selection, plasticity and maternal effects in this trait-environment association. Transgenerational effects were studied by planting offspring of inbred maternal families grown in both environments across the same environments in the second year. Reciprocal transplants revealed local adaptation to habitat type: broad-leaved forms had higher fitness in oak understory and linear-leaved plants had higher fitness in open grassland habitat. Phenotypic selection analyses indicated selection for narrower leaves and lower SLA in open habitat, and selection for broad leaves and intermediate values of SLA in understory. Both plant morphs exhibited plastic responses in traits in the same direction as selection on traits (narrower leaves and lower SLA in open habitat) suggesting that plasticity is adaptive. We detected an adaptive transgenerational effect in which maternal environment influenced offspring fitness; offspring of grassland-reared plants had higher fitness than understory-reared plants when grown in grassland. We did not detect costs of plasticity, but did find a positive association between leaf shape plasticity and fitness in linear-leaved plants in grassland habitat. Together, these findings indicate that fixed differences in trait values corresponding to selection across habitat contribute to local adaptation, but that plasticity and maternal environmental effects may be favored through promotion of survival across heterogeneous environments.     

Offspring fitness in relation to population size and genetic variation in the rare perennial plant species Gentiana pneumonanthe (Gentianaceae)

Seeds were sampled from 19 populations of the rare Gentiana pneumonanthe, ranging in size from 5 to more than 50,000 flowering plants. An analysis was made of variation in a number of life-history characters in relation to population size and offspring heterozygosity (based on seven polymorphic isozyme loci). Life-his-tory characters included seed weight, germination rate, proportion of seeds germinating, seedling mortality, seedling weight, adult weight, flower production per plant and proportion of plants flowering per family. Principal component analysis (PCA) reduced the dataset to three main fitness components. The first component was highly correlated with adult weight and flowering performance, the second with germination performance and the third component with seed and seedling weight and seedling mortality. The latter two components were considered as being maternally influenced, since these comprised life-history traits that were significantly correlated with seed weight. Multiple regression analysis showed that variation in the first fitness component was mainly associated with heterozygosity and not with population size, while the third fitness component was only correlated with population size and not with heterozygosity. The latter relationship appeared to be non-linear, which suggests a stronger loss of fitness in the smallest populations. The second (germination) component was neither correlated with population size nor with genetic variation. There was only a weak association between population size, heterozygosity and the population coefficients of variation for each life history character. Most correlation coefficients were negative, however, which suggests that there is more variation among progeny from smaller populations. We conclude that progeny from small populations of Gentiana pneumonanthe show reduced fitness and may be phenotypically more variable. One of the possible causes of the loss of fitness is a combination of unfavourable environmental circumstances for maternal plants in small populations and increased inbreeding. The higher phenotypic variation in small populations may also be a result of inbreeding, which can lead to deviation of individuals from the average phenotype through a loss of developmental stability.     

Seed number and environmental conditions do not explain seed size variability for the invasive herb Lupinus polyphyllus

Intraspecific variation in seed size may result from life-history constraints or environmental conditions experienced. This variation in seed size is likely to affect the early stage of invasion as seed size may contribute to the success or failure of population establishment. However, only a few studies have examined seed size variability and its causes and consequences for invaders so far. Using the invasive herb Lupinus polyphyllus, we estimated seed mass variation within and among 39 populations from two different geographic regions in a part of the invaded range. We empirically and experimentally evaluated the effect of seed number and environmental conditions (e.g. geographic region, habitat type, intraspecific competition) on seed mass, emergence and seedling performance. Seed mass varied threefold, being largest among individual plants within populations and smallest among populations. Variation in seed mass was neither related to seed number nor the environmental conditions examined, but led to differences in offspring performance, with emergence and seedling size increasing with seed mass. Larger L. polyphyllus seeds were better establishers than smaller seeds regardless of environmental conditions, indicating that the success of L. polyphyllus invasions is likely to depend positively on seed mass. Our results suggest that some plant species such as the invasive L. polyphyllus may not show an adaptive response in seed mass to resources or environmental conditions, which may partly explain their ability to colonise a range of different habitats.     

Maternal investment in egg size: environment- and population-specific effects on offspring performance

Geographic variation in maternal investment in offspring size can be adaptive if differences in investment translate into improved offspring performance in the given environments. We compared two moor frog, Rana arvalis, populations in the laboratory to test the hypothesis that investment in large eggs in populations originating from stressful (acid) environments improves offspring performance when reared in stressful (acid) conditions. We found that large initial size (hatchling mass) had moderate to strong, environment-dependent positive effects on larval and metamorphic traits in the acidic origin population, but only weak effects in the neutral origin population. Our results suggest that interactions between environmental conditions and initial size can be important determinants of individual performance, and that investment in large eggs is adaptive in acid environments. These findings emphasize the role of maternal effects as adaptations to environmental stress.