The role of maternal effects in adaptation to different diets

The environmental influences of mothers on offspring traits, or maternal effects, often arise from dietary differences experienced by mothers. However, few studies have explored if and how maternal effects facilitate adaptation to new host plants. To address this, we compared the maternal and direct effects arising from dietary differences in two populations of the large milkweed bug, Oncopeltus fasciatus that live on and feed on the seeds from different hosts. We compared a laboratory population, which has been reared for over 400 generations on sunflower seeds and is now adapted to use these as a host, to the wild population, which is adapted to the ancestral diet of toxic milkweed seeds. We first tested for changes in maternal effects, and then examined offspring performance and survivorship. We found evidence for evolution of the maternal effect facilitating the use of a novel host. However, the strongest effects were population differences and direct dietary effects for all traits. Offspring performance was more strongly influenced by diet than maternal effects. Survivorship depended on population and offspring diet, and their interaction, but was unaffected by maternal diet or other interactions. In the artificially evolved population, diet breadth was increased rather than evolving specialization. Our results suggest changes in maternal effects are likely to be weak compared to direct effects of host plants and other adaptations in adaptation to a novel host. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 114 , 202–211.     

克隆和有性亲体效应及其调控机制

植物表型受自身基因型、所处环境及其亲体所经历环境的共同影响;其中,亲体环境对子代表型的影响被称为亲体效应。亲体效应不仅可通过有性繁殖产生的种子传递给后代(即有性亲体效应),也可以通过克隆生长等无性繁殖产生的分株传递给后代(即克隆亲体效应)。亲体效应对植物种群,特别是对有性繁殖受限、缺乏遗传变异的克隆植物种群的长期进化可能发挥着极其重要的作用,因此,对亲体效应研究进展的梳理非常必要。对克隆亲体效应和有性亲体效应的内涵进行了阐释,并论述了克隆和有性亲体效应对子代表型、适合度、种内/种间竞争能力以及种群/群落结构和功能的潜在影响;阐述了亲体效应的潜在调控机制,包括供给机制、代谢物质调控机制、表观遗传机制等;论述了克隆亲体效应在克隆植物适应进化中的作用。未来可以就克隆亲体效应的遗传稳定性及其对克隆生活史性状变异的贡献程度,以及克隆和有性亲体效应引起的表型多样性对种内/种间关系、种群/群落多样性及生态系统结构、功能和稳定性的影响开展深入研究。     

Complex environmental effects on the expression of alternative reproductive phenotypes in the bulb mite

Understanding the evolution and maintenance of within-sex reproductive morphs, or alternative reproductive phenotypes (ARPs), requires in depth understanding of the proximate mechanisms that determine ARP expression. Most species express ARPs in complex ecological environments, yet little is know about how different environmental variables collectively affect ARP expression. Here, I investigated the influence of maternal and developmental nutrition and sire phenotype on ARP expression in bulb mites (Rhizoglyphus robini), where males are either fighters, able to kill other mites, or benign scramblers. In a factorial experiment, females were raised on a rich or a poor diet, and after maturation they were paired to a fighter or a scrambler. Their offspring were put on the rich or poor diet. Females on the rich diet increased investment into eggs when mated to a fighter, but suffered reduced longevity. Females indirectly affected offspring ARP expression as larger eggs developed into larger final instars, which were more likely to develop into a fighter. Final instar size, which also strongly depended on offspring nutrition, was the main cue for morph development: a switch point, or size threshold, existed where development switched from one phenotype to the other. Sire phenotype affected offspring phenotype, but only if offspring were on the poor diet, indicating a gene by environment interaction. Overall, the results revealed that complex environmental effects can underlie ARP expression, with differential maternal investment potentially amplifying genetic effects on offspring morphology. These effects can therefore play an important role in understanding how selection affects ARP expression and, like quantitative genetics models for continuous traits, should be incorporated into models of threshold traits.     

PATERNAL CARE: DIRECT AND INDIRECT GENETIC EFFECTS OF FATHERS ON OFFSPRING PERFORMANCE

Knowledge of how genetic effects arising from parental care influence the evolution of offspring traits comes almost exclusively from studies of maternal care. However, males provide care in some taxa, and often this care differs from females in quality or quantity. If variation in paternal care is genetically based then, like maternal care and maternal effects, paternal effects may have important consequences for the evolution of offspring traits via indirect genetic effects (IGEs). IGEs and direct–indirect genetic covariances associated with parental care can contribute substantially to total heritability and influence predictions about how traits respond to selection. It is unknown, however, if the magnitude and sign of parental effects arising from fathers are the same as those arising from mothers. We used a reciprocal cross‐fostering experiment to quantify environmental and genetic effects of paternal care on offspring performance in the burying beetle, Nicrophorus vespilloides. We found that IGEs were substantial and direct–indirect genetic covariances were negative. Combined, these patterns led to low total heritabilities for offspring performance traits. Thus, under paternal care, offspring performance traits are unlikely to evolve in response to selection, and variation in these traits will be maintained in the population despite potentially strong selection on these traits. These patterns are similar to those generated by maternal care, indicating that the genetic effects of care on offspring performance are independent of the caregiver's sex.     

COMPLEX INTERACTIONS BETWEEN PATERNAL AND MATERNAL EFFECTS: PARENTAL EXPERIENCE AND AGE AT REPRODUCTION AFFECT FECUNDITY AND OFFSPRING PERFORMANCE IN A BUTTERFLY

Parental effects can greatly affect offspring performance and are thus expected to impact population dynamics and evolutionary trajectories. Most studies have focused on maternal effects, whereas fathers are also likely to influence offspring phenotype, for instance when males transfer nutrients to females during mating. Moreover, although the separate effects of maternal age and the environment have been documented as a source of parental effects in many species, their combined effects have not been investigated. In the present study, we analyzed the combined effects of maternal and paternal age at reproduction and a mobility treatment in stressful conditions on offspring performance in the butterfly Pieris brassicae. Both paternal and maternal effects affected progeny traits but always via interactions between age and mobility treatment. Moreover, parental effects shifted from male effects expressed at the larval stage to maternal effects at the adult stage. Indeed, egg survival until adult emergence significantly decreased with father age at mating only for fathers having experienced the mobility treatment, whereas offspring adult life span decreased with increasing mother age at laying only for females that did not experience the mobility treatment. Overall, our results demonstrate that both parents’ phenotypes influence offspring performance through nongenetic effects, their relative contribution varying over the course of progeny's life.     

Genetic variation for maternal effects on parasite susceptibility

The expression of infectious disease is increasingly recognized to be impacted by maternal effects, where the environmental conditions experienced by mothers alter resistance to infection in offspring, independent of heritability. Here, we studied how maternal effects (high or low food availability to mothers) mediated the resistance of the crustacean Daphnia magna to its bacterial parasite Pasteuria ramosa. We sought to disentangle maternal effects from the effects of host genetic background by studying how maternal effects varied across 24 host genotypes sampled from a natural population. Under low‐food conditions, females produced offspring that were relatively resistant, but this maternal effect varied strikingly between host genotypes, i.e. there were genotype by maternal environment interactions. As infection with P. ramosa causes a substantial reduction in host fecundity, this maternal effect had a large effect on host fitness. Maternal effects were also shown to impact parasite fitness, both because they prevented the establishment of the parasites and because even when parasites did establish in the offspring of poorly fed mothers, and they tended to grow more slowly. These effects indicate that food stress in the maternal generation can greatly influence parasite susceptibility and thus perhaps the evolution and coevolution of host–parasite interactions.     

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.     

Forest Fragmentation and Seed Germination of Native Species from the Chaco Serrano Forest

Habitat fragmentation is a widespread phenomenon that alters pollination and plant reproductive processes. These effects have demographic and genetic implications that determine offspring fitness and the long‐term viability of plant populations in fragmented systems. We evaluated fragmentation effects on early plant offspring fitness traits, individual seed mass, and percentage of seed germination in five native plant species (Acacia caven, Celtis ehrenbergiana, Croton lachnostachyus, Rivina humilis, Schinus fasciculatus) from the Chaco Serrano forest, a subtropical highly fragmented ecosystem. We found evidence of strong negative fragmentation effects on germination in the shrub C. lachnostachyus and the perennial herb R. humilis, after 30 d of controlled tests. No fragmentation effects were found in the studied traits on the remaining three tree species. We found significant maternal effects in offspring fitness traits in all five species. We discuss the relative magnitude of maternal vs. fragmentation effects taking into account both plant species' lifespan and the time elapsed in fragmentation conditions. We emphasize the need to increase the study of early and late plant offspring fitness produced in fragmented habitats coupled with analyses of genetic parameters and the pollination process in order to evaluate the conservation value of remnant forest fragments. Abstract in Spanish is available at http://www.blackwell‐synergy.com/loi/btp .     

Unravelling the effects of differential maternal allocation and male genetic quality on offspring viability in the dung beetle, Onthophagus sagittarius

Good genes models of mate choice assume heritability of fitness-related traits. However, maternal effects can inflate estimates of trait heritability, and genotype-environment interactions can have significant effects on good genes processes of evolution. Thus, partitioning genetic and maternal/environmental sources of variation in studies of good genes mate choice represents an empirical challenge. In this study, we used the dung beetle Onthophagus sagittarius to examine additive genetic and maternal effects on egg-to-adult offspring viability. We used a half-sib full-sib breeding design and manipulated the maternally provided environment by reducing or increasing the mass of the brood ball within which each offspring developed. We found evidence of differential allocation of investment by females in the brood balls they produced. However, experimental manipulations of maternal allocation to brood balls had only a weak and non-significant influence on the sire effects on offspring viability. Significant additive genetic effects on offspring viability were pervasive across our manipulations of the maternally provided larval environment. This finding indicates that although females do show differential allocation to offspring based on sire phenotype, ‘good genes’ benefits of mate choice are not dependent upon differential maternal allocation.     

Effects of maternal age and environment on offspring vital rates in the oleander aphid (Hemiptera: Aphididae)

Maternal effects have the potential to affect population dynamics and evolution. To affect population dynamics, maternal effects must influence offspring vital rates (birth, death, or movement). Here, we explore the magnitude of nongenetic maternal influence on the vital rates of an insect herbivore and explore predictability of maternal effects with reference to published studies. We experimentally studied the effects of maternal age, host plant species (two Asclepias spp.), and density on offspring vital rates in Aphis nerii, the oleander aphid. Older mothers produced offspring that lived shorter lives, consistent with the "Lansing Effect." Older mothers also produced offspring that matured at a younger age. As maternal age increased, offspring mass at maturity decreased when mothers were on Asclepias syriaca. However, offspring mass was highest from intermediate aged mothers on A. viridis. The absence of maternal density effects seems to exclude maternal density as a potential source of delayed density dependence in A. nerii. Our results indicate that maternal effects have some influence on A. nerii vital rates. However, references to published studies suggest that only the Lansing Effect is a predictable response to maternal age in insects. Moreover, the magnitude of observed effects was generally low.     

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.     

Sex dimorphism of life-history traits and their response to environmental factors in spider mites

Sex dimorphism is ubiquitous in the animal kingdom and can be influenced by environmental factors. However, relatively little is known about how the degree and direction of sex difference vary with environmental factors, including food quality and temperature. With the spider mites from the family Tetranychidae as subjects, the sex difference of life-history traits in responses to host plant and temperature were determined in this meta-analytic review. Across the 42 studies on 26 spider mite species (N?=?8057 and 3922 for female and male mites, respectively), female spider mites showed longer developmental duration than the males in all except two species. The direction of sex difference in development was consistent regardless of temperature and host plant. The 16 spider mite species in 33 studies generally showed female-biased longevity, with an overall effect size of 0.6043 [95%CI = 0.4054–0.8031]. Host plant significantly influenced the sex difference in longevity, where the males lived longer than females below 22.5 ℃, but the reverse was true at higher and fluctuating temperature. Host plant also influenced the magnitude of sex difference in longevity, with females living longer than males when reared on herbs but not on trees. This study indicated that life-history traits are highly variable between sexes under temperature and host plant influence, highlighting that environmental conditions can significantly shape the direction and magnitude of sexual dimorphism of life-history traits.

     

Effects of host plant on life‐history traits in the polyphagous spider mite Tetranychus urticae

Studying antagonistic coevolution between host plants and herbivores is particularly relevant for polyphagous species that can experience a great diversity of host plants with a large range of defenses. Here, we performed experimental evolution with the polyphagous spider mite Tetranychus urticae to detect how mites can exploit host plants. We thus compared on a same host the performance of replicated populations from an ancestral one reared for hundreds of generations on cucumber plants that were shifted to either tomato or cucumber plants. We controlled for maternal effects by rearing females from all replicated populations on either tomato or cucumber leaves, crossing this factor with the host plant in a factorial design. About 24 generations after the host shift and for all individual mites, we measured the following fitness components on tomato leaf fragments: survival at all stages, acceptance of the host plant by juvenile and adult mites, longevity, and female fecundity. The host plant on which mite populations had evolved did not affect the performance of the mites, but only affected their sex ratio. Females that lived on tomato plants for circa 24 generations produced a higher proportion of daughters than did females that lived on cucumber plants. In contrast, maternal effects influenced juvenile survival, acceptance of the host plant by adult mites and female fecundity. Independently of the host plant species on which their population had evolved, females reared on the tomato maternal environment produced offspring that survived better on tomato as juveniles, but accepted less this host plant as adults and had a lower fecundity than did females reared on the cucumber maternal environment. We also found that temporal blocks affected mite dispersal and both female longevity and fecundity. Taken together, our results show that the host plant species can affect critical parameters of population dynamics, and most importantly that maternal and environmental conditions can facilitate colonization and exploitation of a novel host in the polyphagous T. urticae, by affecting dispersal behavior (host acceptance) and female fecundity.     

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 warming affects early life stages of an invasive thistle

Maternal environment can influence plant offspring performance. Understanding maternal environmental effects will help to bridge a key gap in the knowledge of plant life cycles, and provide important insights for species’ responses under climate change. Here we show that maternal warming significantly affected the early life stages of an invasive thistle, Carduus nutans. Seeds produced by plants grown in warmed conditions had higher germination percentages and shorter mean germination times than those produced by plants under ambient conditions; this difference was most evident at suboptimal germination temperatures. Subsequent seedling emergence was also faster with maternal warming, with no cost to seedling emergence percentage and seedling growth. Our results suggest that maternal warming may accelerate the life cycle of this species via enhanced early life‐history stages. These maternal effects on offspring performance, together with the positive responses of the maternal generation, may exacerbate invasions of this species under climate change.     

Haemosporidian parasites depress breeding success and plumage coloration in female barn swallows Hirundo rustica

Parasites are major effectors of natural selection and also play a role in sexual selection processes. Haemosporidian blood parasites are common in vertebrates and have been shown to vary in their effects depending on both the parasite and host species, on the host trait investigated as well as on host condition and stage of infection. Here we investigated infection of adult barn swallows Hirundo rustica by Plasmodium, Leucocytozoon and Haemoproteus species during the chronic stage of infection and the consequences for host fitness traits. Prevalence was higher than 10% only for Plasmodium. Chronic stage infection by Plasmodium was associated with reduced female breeding success, but did not affect breeding dates. Infection did not affect the expression of male secondary sexual traits (tail length and melanin‐based plumage coloration), but was associated with paler coloration of females. Finally, we found a negative effect of infection by Plasmodium on feather growth rate in older but not in yearling individuals. Because feathers are moulted during wintering in sub‐Saharan Africa where infection of barn swallows by Plasmodium occurs, our results suggest that male secondary sexual traits have little potential to reveal acute‐stage infection whereas plumage coloration of females may advertise their infection status. In addition, these results suggest that infection by Plasmodium can influence the course of plumage moult. Thus, our results add to the observations of negative effects of haemosporidian infection on fitness traits in birds and provides evidence that these effects can vary among traits and in relation to age and sex.     

Direct and plant trait‐mediated effects of the local environmental context on butterfly oviposition patterns

Variation in the intensity of plant–animal interactions over different spatial scales is widespread and might strongly influence fitness and trait selection in plants. Differences in traits among plant individuals have been shown to influence variation in interaction intensities within populations, while differences in environmental factors and community composition are shown to be important for variation over larger scales. However, little is still known about the relative importance of the local environmental context vs. plant traits for the outcome of interactions within plant populations. We investigated how oviposition by the seed‐predator butterfly Phengaris alcon on its host plant Gentiana pneumonanthe was related to host plant traits and to local environmental variation, as well as how oviposition patterns translated into effects on host plant fruit set. We considered the local environmental context in terms of height of the surrounding vegetation and abundance of the butterfly's second host, Myrmica ants. The probability of oviposition was higher in plants that were surrounded by lower vegetation, and both the probability of oviposition and the number of eggs increased in early‐flowering and tall plants with many flowers in the three study populations. Flowering phenology, shoot height and flower production were, in turn, related to higher surrounding vegetation. Myrmica abundance was correlated with vegetation height, but had no effect on oviposition patterns. Oviposition and subsequent seed predation by the caterpillars strongly reduced host plant fruit set. Our results show that plant–animal interactions are context‐dependent not only because the context influences the abundance or the behavior of the animal interactor, but also because it influences the expression of plant traits that affect the outcome of the interaction. The results also demonstrate that heterogeneity in environmental conditions at a very local scale can be important for the outcomes of interactions.     

PARENTAL EFFECTS ON SEED DEVELOPMENT AND SEED YIELD IN RAPHANUS RAPHANISTRUM: IMPLICATIONS FOR NATURAL AND SEXUAL SELECTION

The possibility that sexual selection operates in angiosperms to effect evolutionary change in polygenic traits affecting male reproductive success requires that there is additive genetic variance for these traits. I applied a half-sib breeding design to individuals of the annual, hermaphroditic angiosperm, wild radish (Raphanus raphanistrum: Brassicaceae), to estimate paternal genetic effects on, or, when possible, the narrow-sense heritability of several quantitative traits influencing male reproductive success. In spite of significant differences among pollen donors with respect to in vitro pollen tube growth rates, I detected no significant additive genetic variance in male performance with respect to the proportion of ovules fertilized, early ovule growth, the number of seeds per fruit, or mean individual seed weight per fruit. In all cases, differences among maternal plants in these traits far exceeded differences among pollen donors. Abortion rates of pollinated flowers and fertilized ovules also differed more among individuals as maternal plants than as pollen donors, suggesting strong maternal control over these processes. Significant maternal phenotypic effects in the absence of paternal genetic or phenotypic effects on reproductive traits may be due to maternal environmental effects, to non-nuclear or non-additive maternal genetic effects, or to additive genetic variance in maternal control over offspring development, independent of offspring genotype. While I could not distinguish among these alternatives, it is clear that, in wild radish, the opportunity for natural or sexual selection to effect change in seed weight or seed number per fruit appears to be greater through differences in female performance than through differences in male performance.     

Effects of the maternal and pre‐adult host plant on adult performance and preference in the pea aphid,Acyrthosiphon pisum

Abstract 1. The taxon known as the pea aphid, Acyrthosiphon pisum, is composed of a series of host plant associated populations and is widely used as a model system to explore ecological speciation and the evolution of specialisation. It is thus important to know how maternal and pre‐adult experience influences host plant utilisation in this species. 2. The relative importance of the maternal and pre‐adult host plant for adult fecundity and host preference was investigated using three aphid clones collected from Lathyrus pratensis and maintained on Lathyrus or Vicia faba. 3. No significant effects of the maternal host plant on offspring fecundity were detected. 4. The host plant on which the aphid grew up influenced adult fecundity, although in a complex way that depended on both the adult host plant species and when after transfer to the test plant fecundity was assessed. 5. All three clones preferred to colonise Lathyrus over Vicia, and this preference was stronger for aphids raised on Lathyrus. 6. The significance of the results for studies of the evolution of specialisation and speciation that employ A. pisum is discussed.     

Selection response in traits with maternal inheritance

Maternal inheritance is the non-Mendelian transmission of traits from mothers to their offspring. Despite its presence in virtually all organisms, acting through a variety of mechanisms, the evolutionary consequences of maternal inheritance are not well understood. Here we review and extend a model of the inheritance and evolution of multiple quantitative characters with complex pathways of maternal effects. Extensions of the earlier model include common family environmental effects not associated with maternal phenotype, sexual dimorphism, and paternal effects (non-Mendelian influence of the father on offspring traits). We find that, in contrast to simple Mendelian inheritance, maternal inheritance produces qualitatively different evolutionary dynamics for two reasons: (1) the response to selection on a set of characters depends not only on their additive genetic variances and covariances, but also on maternal characters that influence them, and (2) time lags in the response to selection create a form of evolutionary momentum. These results have important implications for evolution in natural populations and practical applications in the economic improvement of domesticated species. We derive selection indices that maximize either the economic improvement in a single generation of artificial selection or the asymptotic rate of improvement in long-term selection programmes, based on individual merit or a combination of individual and family merit. Numerical examples show that accounting for maternal inheritance can lead to considerable increases in the efficiency of artificial selection.