incidence and consequences of inherited environmental … · · 2017-08-16incidence and...

September 20, 1996 20:59 Annual Reviews ROSSCHPT.DUN AR019-15

Annu. Rev. Ecol. Syst. 1996. 27:451–76Copyright c© 1996 by Annual Reviews Inc. All rights reserved

INCIDENCE AND CONSEQUENCESOF INHERITED ENVIRONMENTALEFFECTS

MaryCarol RossiterInstitute of Ecology, University of Georgia, Athens, Georgia 30602

KEY WORDS: maternal effects, nongenetic cross-generational transmission, non-Mendelianinheritance, paternal effects, time-lagged components of phenotypic variance

ABSTRACT

Inherited environmental effects are those components of the phenotype that arederived from either parent, apart from nuclear genes. Inherited environmentaleffects arise as the product of parental genes and the parental environment, ortheir interation, and can include contributions that reflect the abiotic, nutritional,and other ecological features of a parental environment. Separating the impactof inherited environmental effects from inherited genetic effects on offspringphenotype variation has been and continues to be a challenge. This complexityis represented in the presentation of a qualitative model that distinguishes thepossible paths of nongenetic cross-generational transmission. This model servesas the framework for considering the nature, in published works, of what wasactually measured. Empirical evidence of inherited environmental effects arisingfrom these pathways is documented for a diversity of plant and animal taxa.From these results one can conclude that the impact of inherited environmentaleffects on offspring can be positive or negative depending on the nature of thecontribution and the ecological context in which the offspring exists. Finally,there is a description of theoretical and experimental efforts to understand theconsequences of parental effects relative to their impact on population dynamics,the expression of adaptive phenotype plasticity, and character evolution.

INTRODUCTION AND TERMINOLOGY

Inherited environmental effects include those components of an offspring’sphenotype that are derived from the parent, apart from the nuclear genes. Thisdefinition serves as the broad designation for the outcome of multiple cross-

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generational processes described in the following section. In this review, youwill see that inherited environmental effects are documented for species from abroad taxonomic range, and that the external parental environment often playsa significant role in the magnitude and nature of the expression of these effects.Moreover, most of the parental environmental variables known to contributeto inherited environmental effects are permanent components of species’ envi-ronments (e.g. seasonal features, density, or food and habitat quality); this factsuggests their sustained importance in ecological and evolutionary processes.Much of the work that addresses the complexity of transmission of inheritedenvironmental effects uses quantitative genetic analysis. I hope to distill, butnot to minimize, this complexity by including a general framework that pro-vides a way to think about how previous environmental experience interactswith genes to alter individual and population responses in unexpected ways.

Since an array of terms are used for the processes involved in inheritedenvironmental effects, I first define those used frequently. The most commonand most variably defined are “maternal effects” and “paternal effects.” Thesedesignations include the inheritance of nuclear genes from the mother or father(84, 134, 211), the inheritance of cytoplasmic genes (mitochondria or plastids)from the mother or father (95, 134), or the transmission of information derivedfrom parental quality or parental environment (11, 40, 116, 161). Sometimesthese terms are used without distinguishing the source of impact on offspringphenotype. For example, the presence of a maternal or paternal effect is inferredwhen offspring from reciprocal crosses differ in mean phenotype (68, 150, 157,184, 190).

The term “maternal genetic inheritance” or “maternal additive inheritance”is used when a component of the maternal effect is of genetic origin, that is,due to maternal performance genes expressed in the mother and received as anenvironmental component of offspring phenotype. After the maternal geneticeffects are accounted for, the remainder of the inherited environmental effect isoften called a “maternal environmental effect” (40, 50, 56, 160, 217, 218). Whenconfirmation of nongenetic cross-generational transmission arises (e.g. fromvariation in the parental environment due to photoperiod or nutritional quality),the terms “environmentally based” maternal, paternal, or parental effects (69,168) and “general environmental” and “specific environmental” maternal orpaternal effects (180) are used, depending on the experimental design. Durrant(51) found that flax varieties grown under several nutrient regimes respondedwith changes in their own growth parameters and appeared to transmit thesechanges to their offspring in the next and later generations, a phenomenon hecalled maternal “conditioning.”

Inherited environmental effects that extend beyond one offspring generationare called “permanent” (218) or “persistent” (160) environmental effects. For


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example, an environmental effect on a grandmother’s maternal performance in-fluences the maternal performance of her daughter and thus affects phenotypicvalues in grandchildren, and so on (56). Multiple generation reverberation isalso called “environmental inheritance” because the maternal performance phe-notype of the mother can directly modify the maternal performance phenotypeof the daughter, even in the absence of genetic heritability (160).

To facilitate discussion of the evolutionary impact of inherited environmen-tal effects, Kirkpatrick & Lande (91) used the term “maternal inheritance”for the transmission of non-Mendelian contributions from parent to offspring,and “maternal selection” for the effect of this transmission on offspring fit-ness. Similarly, Lombardi (109) suggested that “maternal influence,” whichis the equivalent of “maternal inheritance,” should refer to the source ratherthan to the phenotypic impact on offspring expressing inherited environmentaleffects.

PROCESSES THAT PRODUCE INHERITEDENVIRONMENTAL EFFECTS

The multiplicity of meanings and underlying assumptions encompassed by theterm “maternal effects” likely arises from difficulties in (a) distinguishing in-herited environmental effects from direct genetic effects (i.e. transmission ofnuclear genes to offspring), and (b) determining the extent to which inheritedenvironmental effects are mediated by the parental genotype. Some of thiscomplexity is represented in Figure 1, which is based on a quantitative geneticsmodel with inherited environmental effects and a variable offspring environ-ment of Eisen & Saxton (53). This figure differs from their model by the additionof a variable parental environment, a condition often measured or manipulatedin empirical studies of inherited environmental effects. To describe the pro-cesses involved in the production of inherited environmental effects, it is best tostart with the offspring phenotype, then consider what sources may contributeto it.

In Figure 1, offspring phenotype Po may derive from any or all of eightsources shown. Since this figure represents the involvement of only one (ei-ther) parent, interactions between maternal and paternal sources (e.g. as occurin plant endosperm) are not addressed. The source of a contribution to offspringphenotype is indicated as genetic (G) or environmental (E), originating in theparental (m) or offspring (o) generation. The parental performance pheno-type, Pm(t), represents those traits related to the quality of parenting. Pm arisesfrom parental genes for performance traits, Gm(t−1), whose expression can bemodified by the parental environment, Em(t−1) or offspring environment, Eo(t).


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Figure 1 The components of offspring phenotype (Po) expressed in timet, deriving from thedirect contribution of nuclear genes by one parent (Go), a time-lagged presentation of the parentalenvironment (Em), a time-lagged expression of parental performance genes (Gm) and their inter-actions with the parental environment to produce the parental performance phenotype (Pm), plusthe offspring’s own environment (Eo). For simplicity of presentation, G indicates additive geneticeffects with dominance and epistasis assumed to be negligible. The numbered sources indicatepossible routes of contribution to the offspring phenotype; Source 8 is any genetic covariance (cov)between genes expressed in two generations such as covGmGo or cov(GmEo)(GoEo); see text forfull description of variables.

The contributions to offspring phenotype typically considered come from:source 1, the offspring genotype, VGo, which arrives as some fraction (usually,but not always 1/2) of the parental genotype; source 2, the offspring environ-ment, VEo; and source 3, interaction between offspring genotype and offspringenvironment, VGoEo. Modification of offspring phenotype due to inherited en-vironmental effects comes from sources 4 through 8: source 4, contributionof the parental performance phenotype to offspring phenotype due to parentalperformance genotype, VGm (4a); interaction between the parental performancegenotype and parental environment, VGmEm (4b); interaction between parentalperformance genotype and offspring environment, VGmEo (4c); or interactionbetween parental performance genotype, parental environment, and offspringenvironment, VGmEmEo(4d); source 5, contribution of the parental environment,



VEm; source 6, the interaction between parental and offspring environment,VEmEo; source 7, interaction between parental environment and offspring geno-type, VGoEm; and source 8, covariance (correlation) between parental perfor-mance genes expressed in the parental (t− 1) and in subsequent (t, t+1. . . )generations. Here, covariance can be simple, covGmGo, or associated withinteraction effects, e.g. cov(GmEo)(GoEo). The contribution of these covari-ance components to offspring phenotype can be positive or negative, a featureof great consequence in interpreting experimental results and predicting theconsequences of inherited environmental effects (6, 91, 160, 218).

There is empirical evidence for each of these sources, although a singleexperimental design seldom assesses all of them: Source 4a: References 98,142, 180 (plants), 35 (rotifers), 153 (guppies), 6, 43 (mammals); source 4b:38, 98, 142, 145, 180 (plants), 89 (insects), 35 (rotifers), 64 (daphnia), 9, 165(rodents), 107 (fish); source 4d, specifically: 180 (inferred, plants), 107 (fish);sources 4c, 4d, or 6: 1, 60, 124, 125, 180, 182, 198, 220 (plants), 58, 59, 65,66, 67a, 89, 92, 168, 212 (insects), 24 (daphnia), 20 (voles), 87 (frogs), 74, 107(fish), 29 (cattle); source 5: 180 (plants), 78 (insects), 9 (rats); source 7: 98(plants); source 8: 19 (insects), 6, 160, 192, 217 (mammals).

While this model can act as a guide to considering the processes involved inthe expression of inherited environmental effects, an additional complexity mustbe recognized. It is often difficult to assess the presence, source, or magnitudeof inherited environmental effects (a) when selection acts on the gametophyte,which means that selection acts on the parental genotype, a situation that cangive the appearance of inherited environmental effects, or (b) when selectionacts during the embryonic stage, a situation often difficult to measure (59, 194).Experiments can be designed to distinguish (60, 119a) or minimize (102, 103,147, 173, 208) the confounding effects of selection on the measurement ofinherited environmental effects.

HOW THE PARENTAL ENVIRONMENT PARTICIPATES

In addition to direct nuclear and cytoplasmic genetic contributions, parentscan provide offspring with nutrients. This aspect of inherited environmentaleffects is the most extensively studied. Data on egg and seed quality often comefrom studies of parental resource allocation patterns and tradeoffs betweenpropagule size and number, long-standing topics in the study of life-historyevolution (12, 37, 76, 153, 183, 188, 191, 201, 210a). Tools and techniquesfor quantification and manipulation (e.g. 10) provide a tractable approach tostudying this aspect of inherited environmental effects. In addition to nutrients,parents can provide offspring with a preregulated genome, defensive agents,symbionts, pathogens, toxins, hormones, enzymes, and cultural conditioning.Depending on the species, parental environmental contributions can be limited


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to gamete packaging (egg or seed production) or extended through prenataland postnatal periods of care. What follows is a sampling of references thatillustrate each type of environmental participation.

Parental ImprintingThe notion that the environment might determine regulation in a gameticgenome was suggested by Giesel from work onDrosophila(61). He offeredthat a photoperiod-induced paternal effect on offspring development time mightbe attributed to “memory effects” in the male germline arising from changes insome aspect of gene regulation. Since that time, considerable work has beendone on parental imprinting wherein the expression of a gene (or an entireparental genome) in the offspring varies according to its maternal or paternalorigin (210b). It has been argued that DNA methylation (which determines theexpression or repression of a gene) is the mechanism of regulatory modification(8, 115, 199). To support this argument, Barlow (8) developed a model that as-sumes that regulatory modifications occur during gametogenesis because thatis the only period when maternal and paternal gametic genomes are separateand can be subjected to different influences. Since methylation patterns are her-itable, it is reasonable to consider that any environmental influences on DNAmethylation patterns in gametes could result in inherited environmental effects.In the absence of any empirical work, Jablonka & Lamb (80) developed a modelwherein an environmental stimulus induces heritable chromatin modificationsthat are specific and predictable, and which might result in an adaptive responseto the environmental stimulus.

Nutritional Factors in the Parental EnvironmentThe availability of nutrients in the parental generation is known to influenceoffspring phenotype. For example, minerals such as iron and zinc are taken upfrom the parental diet and transmitted to eggs (insects) or developing embryos(rodents) (108, 202). In some insect species, the male provides the femalewith nuptial gifts such as prey items or products of his accessory glands (17)which provide energy sources (104, 114) and minerals (54, 141). While thesegifts may be used by the female for her own needs, there have been numerousconfirmations that the paternally derived materials end up in the egg itself (17).

In species with extended maternal care, the nutritional status of the motherduring prenatal and postnatal care can influence offspring phenotype. In labo-ratory rats, the impact of alcohol intake by mothers on fetal development wasmodified by the quality of her nutrition during pregnancy, such that the negativeeffects of alcohol ingestion on offspring were greater when the mother had alow-protein diet (209). In wild squirrels, juveniles born to mothers who re-ceived supplemental food (sunflower seeds left daily at burrow entrances) were



28% heavier compared to offspring of untreated mothers (owing to faster growthversus longer development time), and this mass difference was maintained afterjuveniles left the natal burrow (205).

Abiotic and Ecological Factors in the Parental EnvironmentThe parental thermal experience can influence cold acclimation of offspring inplants (145) and cold tolerance of offspring inDrosophila(213). Density of theparental population can influence yolk quality in quail (7) and early behaviorof offspring in tent caterpillars (216). From correlations between temporal orspatial environmental heterogeneity and variable provisioning of eggs or seedsby a mother, it has been argued that variable provisions increase the probabilityof maternal fitness when habitat quality for emerging young is unpredictable(e.g. 47, 153).

Defensive AgentsPlant secondary compounds can be sequestered by either parent and passedon to offspring where they serve to defend offspring against natural enemies.Paternal contributions of plant-derived alkaloids are made to offspring in moths(52, 72), butterflies (28), and grasshoppers (22), and terpenoid contributionsare made in moths (30).

SymbiontsWhether the transmission of symbionts across generations is a form of genetic orenvironmental inheritance depends on point of view (111). Beyond the familiarcases of mitochondria and chloroplast and other plastid transmission, other ex-amples may be more pertinent to inherited environmental effects. For example,many marine and terrestrial animal species harbor vertically transmitted bacte-rial or algal symbionts. The influence of these symbionts on offspring vigor canrange from mild to complete (31, 204). Cytoplasmically inherited bacteria canbe transmitted to offspring from either parent (e.g. 27, 195). In some species,cytoplasmically inherited bacteria interfere with paternal chromosome incorpo-ration into fertilized eggs and cause reproductive incompatibility (an exampleof selection on the parental genotype), or the bacteria prevent segregation ofchromosomes in unfertilized eggs and cause parthenogenesis (196, 197). Inthese cases, normal sexual reproduction can be reinstated by treatment withantibiotics (23b, 32, 48, 156, 195). Given this potential for “curing,” the trans-mission of these symbionts through a lineage might be changed in responseto the parental environment, for example, by a diet that includes secondarycompounds from plants or fungi with molecules active against microbes.

Parental Gene ProductsThe parental performance phenotype is responsible for the passage of parentalgene products such as enzymes or proteins (3, 4, 90, 177, 221), hormones


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(77, 130, 136, 163), resistance factors (132), self-made defensive compounds(110), or parental mRNA that is essential for offspring development (usuallyduring the early embryonic period) (13, 88, 155). Whether this transmission issubject to modification by the parental environment is less studied. For insects,the parental photoperiod modifies the hormones that are passed on to offspring inlocusts and aphids (130). Kerver & van Delden (90) suggested that the parentalalcohol experience inDrosophila(i.e. parental environment) may influence thequantity or quality of ADH (or its precursor) passed on. Based on comparisonsof life history and physiology in viviparous fish, Lombardi (109) hypothesizedthat the maternal environmental experience can influence offspring phenotypethrough transfer of disease immunity factors and physiological conditioning ofendocrine, osmoregulatory, and thermoregulatory capacity.

Cultural ConditioningCultural conditioning ranges from the choice of appropriate propagule releasesites in limited care species to teaching/learning phenomena in species withextended parental care (41). For many species with relatively immobile earlystages and no obvious parental care, choice of oviposition site is a compo-nent of the parental performance phenotype, a critical component that deter-mines the first external environment encountered by offspring (148). Choice ofoviposition site, an expression of the parental performance phenotype, can beinfluenced by the quality of the parental environment, for example, faunal com-position of ponds (frogs, 149) and floral composition of fields (insects, 189).Postnatal conditioning results from parental behavior which can have both ge-netic and environmental components. For example, sound reception capacityin infant bats is at least partly determined by the sound reception phenotype ofmothers, and the maternal reception phenotype is dictated, in part, by her ownenvironmental experience (83). In birds, evidence from quantitative geneticanalysis indicates that socially learned foraging-site fidelity is a component ofthe correlation between mother and offspring body size (101). Similarly, lambsshow socially induced preference for the host plants eaten by their mothers(126), as do mice, even when the mother’s food is less palatable than otheravailable food (207).

Toxins and PathogensWhen parental toxicity or infection alters the parental performance phenotype,inherited environmental effects can be expressed. This may or may not involvetransmission of the toxin or pathogen itself. In mice, reciprocal crosses betweenstrains characterized by high and low susceptibility to an encephalitis virus in-dicated that infection was under the influence of the maternal environment (i.e.parental performance phenotype), but not that of the offspring genotype (133).



In molluscs, infectious bacteria from parents were found associated with ga-metes (158). In the Indian meal moth, sublethal viral infection in either motheror father resulted in reduced egg production and hatchability (178). Heavymetals modify grasshoppers’ parental performance phenotype; heavy metalsare also transmitted into eggs, the net effect of which is to modify offspringmetabolism and growth (181). For vertebrates, Lewis (106) provided a com-prehensive medical/occupational hazard reference on the adverse effects on thefitness of offspring of thousands of substances ingested by parents; substancesinclude drugs, food additives, pesticides, metals, and natural plant products.The evidence of inherited environmental effects is enormous, and dependingon the half-life of the ingested substance, reverberations across multiple genera-tions are possible. For example, Swain (200) used data on the half-life of PCBsand the success of their transmission to human offspring through transplacentalpassage and postpartum nursing to predict that PCB transmission would con-tinue for at least five generations based on the intake of just the original mother.

EMPIRICAL EVIDENCE OF INHERITEDENVIRONMENTAL EFFECTS

Most citations in this review come from relatively recent work; citations forearlier work can be found in existing reviews on maternal effects. These re-views include examples of maternal and paternal genetic effects that contributeto the parental performance phenotype, non-nuclear genetic effects, and contri-butions from the parental environment: 67b, 97, 161, 176 (plants); 17, 96, 130,131 (insects); 109, 151 (fish); 86 (amphibians); 186 (reptiles); 42 (mammals),11 (viviparous species). Empirical evidence of inherited environmental effectscomes chiefly from studies that determined whether there is a relationship be-tween (a) a specific aspect of the external parental environment and offspringquality at the egg or seed stage, (b) a specific aspect of the external parentalenvironment and postnatal offspring quality, or (c) parental performance phe-notype and offspring quality. In addition, the presence of maternal or paternaleffects has been (d) inferred from breeding experiments, although these lack in-formation about sources of environmental variation in the parental generation,and (e) directly measured after premature separation of mothers and offspringby embryo transplant and cross-fostering.

Parental Environment and Offspring Quality at Eggor Seed StageEarly fitness traits, particularly propagule quality, are those most likely to ex-press inherited environmental effects (118, 130, 161, 162, 215). Propagule size,often correlated with the level of nutritional provisions supplied to offspring


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(18, 119), can contribute to offspring fitness throughout development (119,167, 169, 198). Egg or seed qualities are desirable traits for experimental workbecause it is often easiest to quantify an inherited environmental effect, par-ticularly the parental environmental component, before the influence of theoffspring environment dominates; some examples are given in Table 1.

Parental Environment and Postnatal Offspring QualityFor plants, invertebrates, and vertebrates, excellent demonstrations exist of thedegree to which the environment in one generation can influence individual andpopulation quality of the next generation. The examples in Table 2 come fromexperiments that confirm the presence and magnitude of inherited environmen-tal effects on postnatal traits when the parental environment was manipulated orits natural variation accounted for. In most cases, the experimental designs pre-vented (or minimized) the possibility that offspring phenotypic patterns weredue to selection during the parental generation. The abbreviation of experi-mental results seen in Table 2 bypasses the creativity and complexity of theseexperimental designs and analyses. (Original references contain full details;particularly recommended are 60, 79, 107, 124, 142, 180, 213.)

Parental Performance Phenotype and Offspring QualityIn contrast to the previous studies in which variation in the external parental en-vironment was measured or manipulated, some studies demonstrate inheritedenvironmental effects without accounting for the external parental environ-ment. Some demonstrations are based on a correlation between the parentalperformance phenotype and offspring phenotype, after genetic contributions aretaken into account. For example, a plant’s maternal provisions to the seed can

Table 1 Incidence of inherited environmental effects related to parents’ environmental experience, expressed inpropagule features

Reference Organism Parental environmental variablea Offspring trait with inherited environmental effects

39 Plants temperature seed weight, nutrient constitution, germinability175 Insects foliage phenolic levels egg weight174 Insects host species yolk provisions (mean & variation around)64 Daphnia food rations egg weight152 Fish food rations size, fat reserves (allocation differed by species)153 Fish food rations number, size, fat reserves113 Fish temperature egg weight137 Chickens food rations yolk quality7 Quail density quantity, quality of yolk provisions85 Frogs temperature, food availability egg size

aVariation in the parental environmental variable was accomplished through manipulation or measurement of natural environ-mental variation.



provide an environment so favorable for early growth that inbreeding effects aretemporarily masked (127, 219). Radiolabelling techniques have been used todocument the incorporation of nongenetic ejaculate materials into insect eggs(112, 139, 140). In polychaetes, the quality of the offspring changes in termsof survival and juvenile size as a function of the mother’s age (25, 105). Inechinoderms, experimental alteration of yolk provisions influences early devel-opmental traits, the most interesting of which is the degree of dependence onexogenous food during the pelagic period, an aspect of a species ecology withimplications for life-history evolution (121). In turtles, maternal ability to se-lect a thermally appropriate nest site, relative to egg size, influences the time toreproduction in daughters (166). In birds, parental performance phenotype, interms of foraging behavior, has a significant influence on offspring growth (146).

Other studies that examine the relationship between parental performancephenotype and offspring quality are based on inference from population geneticsprinciples using reciprocal cross designs, sibling analysis, and parent-offspringregression: (215—plants); (143, 214—insects); (203b—frogs); (144, 179—birds); (21, 71—wild rodents).

Embryo transplantation or cross-fostering experiments have been used toassess the relative contributions of temporally disjunct aspects of the parentalperformance phenotype on offspring phenotype. For example, Cowley et al (44)showed that regardless of offspring genotype, mice transferred as embryos tothe uterus of mothers from an inbred line with large body size had greater bodyweights, longer tails, and higher growth rates compared to those transferredto mothers from an inbred line with small body size. Bolton (18) showed thatalthough egg size was a component of the maternal performance phenotypethat made significant contributions to chick fledgling success, parental careduring nesting was of greater importance. Further documentation of inheritedenvironmental effects stemming from prenatal and postnatal care can be foundin (5, 34, 120—rodents) and (167—turtles).

ECOLOGICAL AND EVOLUTIONARYCONSEQUENCES

Inherited environmental effects influence survival and fecundity, particularlyat the earliest stages of offspring life, a time when mortality and selection areoften greatest (154, 215). By virtue of cross-generational transmission, inher-ited environmental effects may delay the impact of environmental factors onpopulation growth and delay the opportunity for selection to act on the parentalperformance phenotype and the offspring genotype. These considerations haveled to the development of hypotheses and models to predict the consequences


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Table 2 Incidence of inherited environmental effects related to parents’ environmental experience, expressedthrough postnatal stages.

Reference Organism Parental environmental variablea Offspring trait with inherited environmental effectsb,c

2 Plants altitude frost hardiness142 competition intensity seed weight, time to germination, dormancy69 field vs lab resin production60 habitat productivity flower production, plasticity (#)193 microhizal infection or not germination, vegetative & reproductive yield94 microrhizal infection or not development, nutrient content, reproductive allocation124 nutrients, pulse intensity, timing spike biomass for both species tested (#)67b photo period seed germination206 seasonality salt tolerance variables220 soil nutrients seed weight, growth (#)198 soil nutrients seed and plant size (#)1 soil nutrients seed weight, survival & size under nutrient stress180 soil quality seed weight, germination, harvest size (*) (#)38 temperature life history traits through adult stages (#)145 temperature seed weight, nutrient content, cold acclimation98 temperature (pre- post zygotic) seed weight, growth, onset of reproduction(*) (#)78, 79 Insects density at 3 developmental stages degree of gregarization, coloration (*) (#)123 density: pre- & post-natal wingedness117 dietary cadmium hatch success, enzyme activity89 dietary iron availability survival, development time & stability65 deiary quercitin or not development time and weight (#)36 field vs lab development time, diapause, growth variables82 field vs lab heat resistance

(continued)

of inherited environmental effects on ecological and evolutionary processes.In short, it has been predicted that inherited environmental effects can influ-ence population dynamics and character evolution (see below). Clearly, anysignificant changes in population dynamics and character evolution owing toinherited environmental effects will be dependent on ecological circumstanceand the population’s evolutionary history (172).

The consequences of inherited environmental effects will depend on the tran-sience or sustainability of both environmental input and organism response. In-herited environmental effects that are due to transient environmental input comefrom experiences that are unique or intermittent (e.g. toxin spill or drought). Sus-tained environmental input comes from experiences that are predictable such asphotoperiod (61), average temperature (222), successive seasonal change (187,206), or average competition (198). In some cases, the length of a species’ gen-eration time and population structure will determine whether the environmentalsource of an inherited environmental effect is sustained or transient. For exam-ple, the experience of soil contamination by a toxin with a 50-year half-life will



Table 2 continued

Reference Organism Parental environmental variablea Offspring trait with inherited environmental effectsb,c

58 host species survival, development time, body size (*) (#)59 host species survival (#)168 host species & quality pre-dispersal period, development time, pupal weight181 mercury, cadmium in soil hatch, development time, adult weight57 nutritional quality survival, development time164 photoperiod diapause propensity99 photoperiod body weight, temperature sensitivity66 photoperiod age of first reproduction, initial fecundity (#)92 photperiod, temperature diapause propensity23a photoperiod, temperature diapause propensity26 temp, daylength, maternal age diapause propensity67 temperature age of first reproduction, body size (#)223 temeprature body size, territorial success in sons212 temperature cold resistance for both species tested (*) (#)213 temperature cold resistance, development time, fecundity45 temperature heat tolerance73 temperature fecundity35 Rotifers density proportion of mictic offspring107 Fish salinity, food ration time to hatch, hatch success (#)187 Lizards seasonal variation relationship between egg size & survival20 Rodents field density growth rate, age of sexual maturity9 toxin dose survival, development, stress response138 PCB exposure behavior205 food availability initial & subsequent body mass55 pre-reproduc.nutritional quality physiological variables29 Cattle host species pre-weaning size

aSee Footnote a in Table 1.b(*)indicates paternal effect on at least one trait listedc(#)Indicates that offspring response was measured in more than 1 offspring environment

likely be different for a hardwood species than for a soil invertebrate species.Which particular environmental experiences are involved in inherited environ-mental effects will be species-specific or population-specific. Further, the morevariable the magnitude of a sustained environmental input, the more likely willbe the adaptation for buffering through inherited environmental effects (33, 36,46, 75, 107, 122, 129, 169).

Relative to an organism’s response, expression of an inherited environmentaleffect is transient if it is confined to one offspring generation (161). It is moredifficult to decide when transient expression grades into sustained expression.However, multiple-generation reverberation from a single environmental inputis known for plants and animals (38, 94, 125, 171, 181, 200, 212, 218), al-though the intensity usually wanes over time (56, 100). It is conceivable thatan inherited environmental effect is initiated by a transient environmental inputand sustained indefinitely. From a model of parental imprinting that includes


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the environmentally induced regulation of germline genes by DNA methyla-tion, Jablonka & Lamb (80) inferred that inherited environmental effects couldbe responsible for apparent reversible mutations, thus drawing a fine line be-tween genetic and inherited environmental effects. Along similar lines, Koch(93) argues that environmentally induced changes in bacterial gene regulation,including the activation of previously silent genes, are part of an adaptive plas-ticity response in the face of extreme environmental fluctuation.

Population DynamicsInherited environmental effects can generate a delay or acceleration in the re-sponse of a population to its environment. (And the environment can include theorganism’s own phenotype e.g. parental body size or behavior.) It has been hy-pothesized that inherited environmental effects could act as a proximal source oftime-lagged effects on population dynamics, with the potential to cause cyclesor destabilization (either noncyclic outbreak or extinction), depending on otherenvironmental parameters (21, 62, 81, 170, 171, 216). Relative to populationecology, a time lag occurs when the per capita rate of increase of a populationis adjusted by the environment experienced in a previous generation(s). If thetime-lagged component of population growth arises from a t− 2 effect (envi-ronmental experience two generations prior) or greater, population cycles canoccur (14). Inherited environmental effects can produce a time lag of t− 2 orgreater when, for example, they influence fecundity in adult offspring (e.g. 73,168, 193). The capacity of inherited environmental effects to influence popula-tion dynamics is supported by a theoretical model that includes the influence ofpopulation quality expressed on a time delay (62), although the model is equallyapplicable to other proximal sources of time-lagged effects (15, 63). Empiri-cal work, based on extrapolation of laboratory results to the field, supports thehypothesis that inherited environmental effects can influence population dy-namics: (142—plants), (25—polychaetes), (21—lemmings), (20, 135—voles),(224—wild mice), (78, 79, 168, 171, 178—outbreak insect species).

Cross-Generational Phenotypic Plasticityand Life History EvolutionIt has been hypothesized that as the environmental quality becomes less pre-dictable or more heterogeneous, parents will adopt (i.e. selection will favor) astrategy of producing offspring of variable phenotype to increase the probabilityof reproductive success. For example, it has been predicted that inherited envi-ronmental effects will be important to the initial colonization ability of plantsat infertile sites (124), and for early survival in insects with life-history featuresthat preclude or reduce the ability of the parents to place eggs in locations thatwill predictably maximize the probability of future success (172).



Consequently, inherited environmental effects have been characterized as aform of bet-hedging wherein the production of greater phenotypic variation inoffspring phenotype increases the likelihood of survival and reproduction inthe face of environmental uncertainty (33, 36, 122, 185). With bet-hedging,a mother (or father) produces a range of offspring phenotypes, presumably toincrease the probability that some subset of phenotypes will be appropriate forthe environment encountered. The presence of such bet-hedging is interpretedto be a response to unpredictable components of the environment (such as thedegree of annual divergence from seasonal means for temperature and rainfall).Inherited environmental effects have also been characterized as a form of plas-ticity if the parental environmental experience (e.g. photoperiod) produces anaverage adjustment of offspring phenotype which is directional and repeatable(e.g. 36, 203a), or if it produces a change in the magnitude of offspring phe-notypic variation (e.g. 36, 169). Whether inherited environmental effects alterthe magnitude of variance around the offspring mean phenotype or shift theoffspring mean phenotype in a “programmed” direction, there is no certaintythat the effect will be adaptive (i.e. increase the long-term fitness of a lineage),although a positive outcome is often seen (130). Bernardo (11) supplies someexamples of nonadaptive maternal effects in viviparous species and cautionsresearchers about denoting maternal effects as a form of plasticity because theterm contains an adaptive connotation for many.

Boggs (16) is working toward the integration of paternally based inheritedenvironmental effects and life-history evolution. She developed a model topredict the consequences of paternal nuptial gifts on life-history evolution as itrelates to female reproductive allocation of nutrients and the likelihood of sexualselection, mediated by paternal environmental contributions. Data from theliterature corroborated the prediction that male nuptial contributions influencedfemale fecundity only when her feeding was restricted.

Character EvolutionScientists have long been aware of the potential for inherited environmentaleffects to influence evolution. For example, a correlation between the geneticcomponent of the parental performance phenotype and direct genetic effects(source 8 in Figure 1) can accelerate, retard, or change the direction of evo-lution depending on its magnitude and sign (49, 56, 70, 217, 218). Inheritedenvironmental effects can also alter the correlation between offspring genotypeand offspring phenotype (e.g. 36), and thus the response to selection. Evolu-tion will be accelerated or retarded depending on whether sustained inheritedenvironmental effects improve or diminish the relationship between offspringgenotype and phenotype (159). Inherited environmental effects can also pro-duce a delay of one or more generations in the response to selection on the


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parental phenotype. When this time lag occurs, the trajectory of characterevolution cannot be predicted as it would normally be, by defined aspects ofselection pressure and inheritance (91, 100, 160). Kirkpatrick & Lande (91)developed a quantitative genetic model for the evolution of multiple traits un-der maternal inheritance and found that populations could continue to evolvefor an indefinite number of generations after selection was relaxed, and thatthe consequences could be of greater magnitude (+ or −) or in a differentdirection than expected from simple Mendelian inheritance. Under frequency-dependence and maternal selection, wherein response to selection depends ona fitness function and the degree of resemblance between parents and offspring,evolution away from fitness optima is possible.

The results of empirical work lend support to the general prediction thatinherited environmental effects can influence character evolution (128, 198,213). In particular, from a study to estimate the genetic component of bodysize, development time, and propensity to diapause in an herbivorous insect,Carriere (36) discovered that inherited environmental effects can adjust bothamong- and within-family components of variance. He presents data support-ing the contention that a change in the relative magnitude of these variancecomponents (and thus a change in the heritability value) would diminish thepotential for response to selection. Much the same conclusion was drawn byGalloway (60), who did an experiment on an annual herbaceous plant speciesfrom an environment with an unpredictable moisture level. The experimentwas designed to determine how the parental environment influenced offspringphenotype—through selection in the parental generation or through transmis-sion of inherited environmental effects. She found that both processes wereinvolved and concluded from the data that the ability of environmentally basedmaternal effects to reduce phenotypic variation in offspring flower productionwould slow the rate of evolutionary change.

Groeters & Dingle (66) found that response to selection on reproductive traitsin the milkweed bug was modified by a maternal effect; this resulted in a lackof opportunity to select strongly for long delays in the onset of reproductionfor two successive generations. From this result they concluded that inheritedenvironmental effects could constrain adaptation toward a genetic optimumbut, by providing an override mechanism to the genetically based response ofoffspring to some environmental condition, could allow greater realization of aphenotypic optimum.

Lacey (98) subjected the parental generation of an herbaceous perennial plantspecies to several temperature regimes during the pre- and post-zygotic phasesof seed production in order to quantify the relative contributions of genetic andinherited environmental effects at sequential stages of development. In the lightof the results, she describes the potential for evolutionary change in flowering



time based on the direction of the parental effect (parental temperature hastensor slows offspring flower development) relative to the profile of a population’sgenetic variation (frequency distribution of genes for flowering time).

Plantenkamp & Shaw (142) studied an annual plant species where the parentalgeneration was reared under different competition regimes. They found, amongother things, the presence of a Gm × Em interaction (source 4b on Figure 1)for seed weight. From this and other results they discuss the role of inher-ited environmental effects on the evolution of reaction norms for seed weightand suggest that such reaction norms may contribute to the maintenance ofmaternally based genetic variation.

A reading of the papers cited in this section reveals that empirical demonstra-tion of the impact of inherited environmental effects on evolution is challenging,particularly when there are temporal changes in the direction and magnitude oftheir expression (e.g. 179, 198), and the underlying biology is unknown (91).

ACKNOWLEDGMENTS

A sincere thank you is extended to all colleagues (nearly 40) who responded toa letter of inquiry with bibliographic information, copies of work in press, en-couragement, and the occasional joke. I also thank Mark Hunter for discussionand enthusiastic support.

Any Annual Reviewchapter, as well as any article cited in anAnnual Reviewchapter,may be purchased from the Annual Reviews Preprints and Reprints service.

1-800-347-8007; 415-259-5017; email: [email protected]. Visitthe Annual Reviews home pageat

http://www.annurev.org.

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