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The Adaptive Significance of Maternal Effects Timothy A REVIEWS The adaptive significance of maternal effects Timothy A. Mousseau and Charles W. Fox he causes and conse- Recently, the adaptive significance Maternal effects on offspring quences of phenotypic of maternal effects has been development variation among individ- increasingly recognized. No longer are There are numerous reported Tuals are of fundamental maternal effects relegated as simple examples of maternal environ- interest to students of evolution- ‘troublesome sources of environmental mental influences on offspring de- ary ecology because it is this vari- resemblance’ that confound our ability velopment. In many insects, the ation that provides the raw ma- to estimate accurately the genetic photoperiod, temperature, or host terial for natural selection. We are basis of traits of interest. Rather, it has availability experienced by an ovi- accustomed to envisioning an indi- become evident that many maternal positing female will determine the vidual’s phenotype as the result effects have been shaped by the action probability of diapause in her off- of its own genotype plus the en- of natural selection to act as a spring5 (Box 2). In general, fe- vironmental effects experienced mechanism for adaptive phenotypic males that experience short photo- during development. However, in response to environmental heterogeneity. periods, cool temperatures or few recent years, with the increasing Consequently, maternal experience potential hosts (i.e. cues that pre- use of quantitative genetic de- is translated into variation in dict deteriorating environmental signs for the study of life history, offspring fitness. conditions) tend to produce a behavior and development, it is high proportion of diapausing off- becoming evident that individual spring. Although the details of the phenotype is frequently, and some- Tim Mousseau is at the Dept of Biological Sciences, response curve (i.e. the reaction times dramatically, influenced by University of South Carolina, Columbia, SC 29208, norm) have rarely been investi- USA ([email protected]); Chuck Fox is at the the environmental experience of Louis Calder Center of Fordham University, gated, environmentally induced other individuals in the popu- 53 Whippoorwill Rd, Box K, Armonk, maternal effects have been demon- lation. Not surprisingly, most often NY 10504, USA strated for more than 70 insects. (but not exclusively), these inter- ([email protected]). Similarly, environmentally induced individual interactions occur be- maternal effects on seed dor- tween mothers and their offspring. mancy and/or germination have Mothers determine propagule been reported in many plants6,7. In size, where, when and how propagules are dispersed, pro- many cases, maternal photoperiod will influence the prob- tection of young from inclement conditions or predators, ability of seed dormancy, although other cues, including parental care and provisioning to developing young, as crowding, light, interspecific competition, maternal size and well as the attributes of the offspring’s father if mate choice the position of the seed on the maternal plant, have been is operating. In addition, a mother’s experience of the en- shown to exert influence on dormancy or germination. In vironment can lead to variation in her growth (i.e. body most cases, the adaptive significance of maternal effects on size), condition and physiological state that can be trans- diapause and dormancy is obvious: survival during the win- mitted to offspring via cytoplasmic factors (e.g. yolk amount, ter (or summer in hot desert environments) is dependent hormones and mRNAs) in the egg that may directly (via upon the physiological state of the propagule. Dormancy maternal programming) or indirectly (via offspring sensi- and diapause are protective mechanisms that enhance sur- tivity to maternally transmitted factors) influence off- vival during inclement seasons. spring development. The extent to which maternal environ- For insects using seasonal or ephemeral resources, en- ment and behavior influence offspring phenotype and vironmental cues, such as crowding, temperature and photo- fitness will determine the likelihood that such maternal period, are often predictable indicators of the future deterio- effects themselves will be shaped by the action of natural ration of their habitat and impending food shortage. In some selection. insects, females (and sometimes males) respond to their In recent symposia1–3, it has been repeatedly suggested environmental conditions by stimulating the production of that maternal effects often provide a mechanism for adap- winged and/or flight-phenotype progeny, or by influencing tive transgenerational phenotypic plasticity, in which the how sensitive their progeny are to subsequent environmen- environment experienced by the mother is translated into tal conditions8. These flight polymorphisms are best studied phenotypic variation in the offspring, and that this relation- in aphids and grasshoppers but have also been studied in ship can be envisioned (and modeled) as a reaction norm other insects. The production of dispersing progeny often (Box 1). Here, we explore four broad classes of environmen- increases with maternal age, possibly because environmen- tally induced maternal effects that have received consider- tal quality tends to decrease throughout the season, which able attention in recent years: (1) maternal effects on offspring corresponds to increasing maternal age. development, (2) the influence of maternal oviposition be- havior on offspring fitness, (3) maternal effects on propa- Effects of maternal oviposition decisions on offspring gule resources, and (4) the influence of female mate choice Even in species with no direct parental care, when, where on offspring. This review complements a recent TREE article and how mothers place their offspring is often the single by Wolf et al.4 that deals with the genetic complications that greatest determinant of offspring success9. For example, a emerge from maternal effects. female herbivore that places her eggs on an appropriate host TREE vol. 13, no. 10 October 1998 Copyright © 1998, Elsevier Science Ltd. All rights reserved. 0169-5347/98/$19.00 PII: S0169-5347(98)01472-4 403 REVIEWS host-plant availability (which it generally is), then it is ad- Box 1. Maternal effects as transgenerational vantageous for them to produce offspring that are ‘acclima- phenotypic plasticity tized’ to the host on which they have been reared. However, Many maternal effects can be visualized as a reaction norm describing the influ- whether females produce offspring that are acclimatized via ence of maternal environment or behavior on an individual offspring’s phenotype nongenetic effects has rarely been tested, and little evi- (as in the figure). Maternal effects occur when a mother’s phenotype influences dence exists for the acclimatization of host-plant suitabil- her offspring’s phenotype independently of the female’s genetic contributions to ity13,14. More work needs to be done in this area because her offspring. Many maternal effects can be modeled as environmentally modu- lated transgenerational phenotypic plasticity, in which environmental variation (e.g. maternal conditioning of host suitability, if demonstrated temperature, photoperiod and nutrients) experienced by mothers is translated into for any organism, could have profound implications for our phenotypic variation in offspring. Similarly, maternal behavior (e.g. host choice, understanding of host-use evolution of herbivores, host-race oviposition behavior and parental care) will often influence offspring phenotype and formation and sympatric speciation. For example, host ex- fitness. perience often influences oviposition preference of females15 and if host experience also influences larval performance on these hosts, then correlations mediated via linkage dis- equilibrium between oviposition preference and larval per- formance could be maintained in a randomly mating popu- lation through the effect of maternal host experience16. Such epigenetic interactions could result in a runaway process that facilitates rapid local adaptation and, eventually, spe- ciation in systems where maternal-oviposition choices de- termine the environments for offspring development16,17. Progeny sex ratio In addition to affecting progeny survival and growth, where and when a female lays her eggs can affect the prog- eny sex [i.e. environmental sex determination (ESD)]18,19. Progeny sex can be influenced by biotic factors, such as the density of conspecifics, the quality of food resources or even by the quality of mate (biotic ESD). Abiotic factors, such as temperature, pH or photoperiod, can also affect progeny In many cases, maternal effects can be visualized as reaction norms that extend across generations. For example, variation in maternal photoperiod often influ- sex (abiotic ESD). In many species, mothers can manipulate ences the expression of diapause in insects5 and dormancy in plants6, and the or respond to their environment in a manner that suggests temperature of a nest chosen by many female reptiles can influence the sex of off- adaptive adjustment of progeny sex. Perhaps the best stud- spring18,19. Similarly, female choice of male secondary sexual characters can influ- ied examples are in the Hymenoptera (wasps, bees and ants), ence aspects of offspring fitness12,22,40,43, and female host choice by herbivores and parasites can dramatically influence offspring growth and survival17,24,36. In ad- in which females can manipulate
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