Maternal Effects in -Plant Interactions: Lessons From a Desert Seed

Charles W. Fox

Department of Entomology S-225 Agricultural Science Center North University of Kentucky Lexington, KY 40546-0091

Abstract of this variation for the production of new Maternal effects occur when the phenotype strains of agricultural plants and . In or environment of a mother affects the this framework, phenotypic variation among phenotype of her offspring via some individuals (VP) is partitioned into a component mechanism other than the transmission of due to genetic differences among individuals genes. The primary objective of this review is (VG), another due to environmental differences to use examples from my own research on the among individuals (VE), and the interaction interaction between seed and their host between these components, producing the now plants to illustrate how maternal effects standard quantitative genetic relationship VP = influence ecological interactions in nature. I VG + VE + interactions (10, 56). Each of these explain how maternal effects generate many components (VG, VE, and interactions) can be patterns observed in nature. I also discuss how further subdivided into sub-components (such maternal effects may be influenced by the as dominance variation, additive genetic genotypes of females or their progeny and can variation, etc.). This simple framework has thus respond to natural selection and evolve. I proven invaluable for understanding responses will emphasize that maternal effects often of agricultural plants and animals to artificial evolve as mechanisms by which females can selection − the response to selection is easily manipulate the phenotype of their progeny to predicted if you know the magnitude of natural prepare them for environmental conditions that selection and the proportion of phenotypic they will encounter (adaptive cross- variation in a population that is due to genetic generational phenotypic plasticity). differences among individuals. Ecologists working with natural systems also use this Introduction simple framework for understanding selection Early in the 20th century and plant in natural systems, and a large body of breeders developed a simple conceptual literature has blossomed in which techniques of framework within which they could quantify quantitative genetics are applied to non- sources of phenotypic variation within agricultural organisms (review in 56). populations and understand the consequences This conceptual framework is invaluable for cytoplasmic organelles (mitochondria and understanding evolutionary processes in nature chloroplasts) from being considered a maternal because it has focused our attention on analyses effect; they are inherited through mothers but of genetic differences among individuals (the are better classified as traits that are inherited VG in the above equation). Such differences are via non-Mendelian genetic inheritance rather basis for responses to natural selection. In this than as a maternal effect. manuscript I will attempt to convince readers Maternal effects are a fundamental that some types of environmental variation (the consequence of the differences in reproductive VE in the above equation) can also be of biology between males and females – mothers ecological and evolutionary importance. provide much of the environmental context Specifically, I will discuss mechanisms by within which progeny develop and progeny which phenotypes of mothers or the genotypes are expressed (78) while in most environments they experience can affect the organisms males provide little more than small phenotypes of their progeny. Until very gametes. Mothers determine how many recently researchers have rarely considered or resources are allocated to eggs (13, 14, 17), measured the impact of environmental effects what type of resources are allocated to eggs (1), experienced in previous generations on and when and where eggs are laid (57). In some contemporary phenotypic expression (55, 50, taxa mothers even determine the sex of their 51, 52). I will argue here that maternal effects progeny (79). After egg production, mothers produce many of the patterns that we observe generally determine how much parental care in nature and that the study of maternal effects their progeny receive, although fathers provide is very important for understanding the parental care in a few (e.g., 74). All of evolution of many types of ecological these maternal “decisions” are chances for a interactions. Using examples from my own mother’s phenotype or environment to work, I will explain how maternal effects influence the phenotype of her progeny (e.g., generate many patterns observed in nature and 25). how they influence population responses to Maternal effects have been identified across natural selection. I also will discuss how a wide variety of taxa and for a wide variety of maternal effects may be influenced by the traits (50, 51, 52, 61, 62). One of the most genotypes of females or their progeny and can commonly observed maternal effects is the thus respond to natural selection and evolve. I influence of maternal age on the phenotype of will emphasize that maternal effects often her progeny (54). In vertebrates and many evolve as mechanisms by which females can aquatic and marine females tend to manipulate the phenotype of their progeny to produce larger progeny as they get older (e.g., prepare them for environmental conditions that 2), but females of most insect species produce they will encounter (adaptive cross- smaller progeny as they get older (17). The generational phenotypic plasticity). seed beetle Callosobruchus maculatus (Coleoptera Bruchidae) exhibits the typical What are Maternal Effects? insect pattern – older females produce smaller In the simplest terms, maternal effects occur eggs than younger females (Fig. 1a) and when the phenotype or environment of a progeny hatching from these smaller eggs tend mother affects the phenotype of her offspring to have lower survivorship and take longer to via some mechanism other than the reach maturity (Fig. 1b), although they tend to transmission of genes (50, 51, 52). By this mature at roughly the same size as their definition, I exclude the inheritance of genes in siblings that hatched from eggs laid by their example, although the size of egg that a female 0.40 Fed females Starved females lays decreases with increasing age, the rate of 0.38 this decrease varies among females depending on their nutritional status (Fig. 1a). Females 0.36 that have ready access to food and water or 0.34 access to extra mates (from which they obtain nutritional contributions) exhibit a slower 0.32

Egg Width (mm) decline in egg size as they get older (11). This 0.30 influence of maternal nutritional status on egg 0 0.5 1 2.5 3 4.5 5 5.5 6 6.5 7 7.5 8 size translates into effects on progeny growth − Maternal Age (days) progeny hatching from eggs produced by well fed females mature sooner than progeny hatching from eggs laid by food-stressed 38 females (Fig. 1b; 11, 20). Oviposition decisions made by a female, 36 such as where to lay her eggs or how many eggs to lay in a locality, will influence the 34 environment within which her offspring will develop (47, 57). In most seed beetles 32 (Coleoptera: Bruchidae) larvae develop inside a single host seed and are incapable of moving 30 among seeds. Females of many species will Development Time (days) 0 0.5 1 2.5 3 4.5 5 5.5 6 6.5 7 7.5 8 either lay clutches (23) or will readily Maternal Age (days) superparasitize seeds (22; but see 47, 48). Each additional egg that a female lays on a seed Figure 1 (a) Female Callosobruchus maculatus produce progressively smaller eggs as they get older. reduces the amount of resources available for (b) This decline in egg influences the egg-to-adult the larvae (including her progeny) inside the development time of a female's progeny (development seed. Fortunately for the larvae, many species time of female progeny is shown). Note that the rate at have evolved developmental plasticity in which which egg size decreases with age depends on the larvae can mature at a smaller than normal − female's nutritional status egg size decreases more body size when reared under intense larval slowly for females that have access to food (shown) or that obtain multiple ejaculates from males, and this competition (Fig. 2a; but see 46). Thus, when influence on egg size corresponds to a change in females lay multiple eggs per seed their progeny development time. Data from 11 and 20. progeny mature at a smaller size than progeny reared at lower densities (e.g., 15, 19, 27). These smaller progeny produce smaller eggs mother when she was younger (11, 20). Thus, a (and have lower fecundity), which influences maternal effect explains much of the the phenotype of the next generation. In C. phenotypic variation in survivorship and maculatus, progeny hatching from these development time within a single family; smaller eggs eventually mature at a smaller size progeny from older females hatch from smaller (Fig. 2b; 13, 14). In both limbatus and S. eggs and must compensate for their small size pruininus progeny hatching from these smaller by extending development time to eventually eggs extend development time to eventually mature at a normal body size. mature at a normal body size (the size at which Maternal effects can also explain much of the phenotypic variation among families. For Callosobruchus Figure 2 (a) The influence of larval density on body 5.5 mass at adult emergence for the seed beetle, maculatus Callosobruchus maculatus. Similar patterns are 5.0 observed in Stator limbatus and S. pruininus (data from 27). (b) The size of progeny produced by a pair 4.5 of adult C. maculatus is influenced by the density at which the female parent was raised, but not the 4.0 density at which the male parent was raised. L - L is a

Female Mass (mg) female reared at low density crossed to a male reared 3.5 1 3 5 7 9 111315171921 at low density, L - H is a female reared at low density crossed to a male reared at high density, and so forth Larval Density (beetles per seed) (data from 27). (c) For Stator pruininus and S. limbatus, the density at which a female is raised affects the development time of her progeny, but not 5.5 Callosobruchus the size at which those progeny mature (data for S. maculatus pruininus from 19). 5.4 at which their mother was reared. Paternal 5.3 density has no effect of the phenotype of 5.2 progeny in either species (Fig. 2b and 2c).

Body Mass (mg) These experiments demonstrate two points. 5.1 First, maternal oviposition decisions can affect L - L L - H H - L H - H the phenotypes of both their progeny and their Cross grand-progeny; females that lay multiple eggs per seed produce smaller progeny, that in turn 25.0 produce smaller eggs, which in turn affects the 24.5 development time or body size of the grand- progeny. This is a maternal effect. Second, 24.0 even though both Callosobruchus and Stator Stator have very similar life cycles, the two beetles 23.5 pruininus exhibit very different types of maternal effects in response to similar ecological stresses (in 23.0 this case, high larval density). Thus, the form in Development Time (days) L - L L - H H - L H - H which maternal effects are exhibited can vary Cross substantially among organisms (e.g., influences they would have matured if reared at low on development time vs. body size), even when density; Fig. 2c; 15, 19). those organisms are ecologically quite similar. In each case we can demonstrate that these differences in body size (C. maculatus) or Paternal Effects development time (both species of Stator) are Although I will focus on maternal effects in environmental effects inherited through this manuscript, I want to acknowledge that mothers by crossing progeny from lines reared paternal effects (the influence of a father's at high density with lines reared at low density. genotype or environment on the phenotype of In these crosses we observe that the size of C. his progeny) are probably more common in maculatus progeny (at maturation; Fig. 2b) and nature than previously suspected. In most the development time of Stator progeny (Fig. insects, males contribute large ejaculates, 2c) are each influenced entirely by the density spermatophores or other accessory gland secretions to a female during mating (4, 75) conditions and the degree to which mothers and nutrients in these contributions can be influence progeny phenotypes in response to incorporated into eggs or used by females for these environmental conditions may be somatic maintenance (e.g., 3). For example, in influenced by the maternal genotype. both Callosobruchus and Stator, males Environmentally-based maternal effects can contribute ≈ 5% of their body mass to females thus have a genetic component and, if during mating, and these contributions can genetically variable, they can evolve within a have large effects on female fecundity (12, 63- population. 66) and egg size (11). It is likely that the size For example, consider that the size of eggs and composition of these contributions affect laid by a mother generally influences the progeny growth and development in many hatchling phenotype of her progeny. All species but we have not yet explored this issue progeny within a family may hatch from in seed beetles. In some insects, defensive similar sized eggs and thus will exhibit similar chemicals sequestered by males may be phenotypes (such as size at hatching and transferred to progeny via male ejaculates or development time) even though they may be spermatophores (9), potentially protecting genetically quite different from each other. progeny from predators or parasites. To However, egg size, and thus the maternal acknowledge the potential importance of effect, may vary substantially among maternal paternal effects in nature, some authors have genotypes such that the maternal effect can argued that we should replace the phrase evolve in a population. Consider also the “maternal effect” with the more general various environmental influences on the size of “parental effect” (e.g., 42). However, for eggs that a female lays. For example, if a consistency with my previous work and female is food-stressed or very old she may lay because I will not discuss “paternal effects” I smaller eggs that produce smaller progeny. In will use the more widely accepted phrase this case the maternal environment (food level “maternal effects” throughout this manuscript. or age), rather than the maternal genotype, influences the size of eggs that she lays and Genetics and the Evolution thus the phenotype of her progeny. However, of Maternal Effects the extent to which a female responds to Although I have defined maternal effects as environmental variation may depend on her influences of a female's phenotype or genotype, and thus natural selection can result environment on the phenotype of her progeny in the evolution of this environmentally-based that are due to some mechanism other than the maternal effect. Also, the degree to which transmission of genes, maternal effects are not mothers can influence the phenotype of their necessarily independent of maternal or progeny progeny may depend of the genotype of their genotypes. In some cases, the maternal traits progeny, resulting in yet another opportunity that influence the progeny phenotype may be for the evolution of maternal effect. influenced by the maternal genotype (a For a similar example, consider parental genetically-based maternal effect) and can thus care in animals. Progeny phenotypes may evolve in response to natural selection. In other depend on the amount of parental care cases, the maternal traits that influence the received, but the amount of parental care progeny phenotype may be influenced by the exhibited by mothers may vary substantially maternal environment (an environmentally- among maternal genotypes. Thus, changes in based maternal effect; 42). However, the maternal genotypes may influence the response of females to their environmental phenotype of progeny via changes in the maternal effect, even if those genes are not When the genes affecting the maternal expressed by progeny. Parental care may also effect are different from the genes affecting the vary with maternal nutritional status or age (an phenotype of progeny, we can observe epistasis environmentally-based maternal effect), between the genes influencing the maternal although the degree to which females change effect and the genes influencing the progeny their parental care in response to environmental traits (78). We can think of the genes that stress or maternal age may vary among female influence maternal effects as the genes that genotypes and also evolve in response to influence the progeny environment, such that natural selection. interactions between maternal and offspring Maternal effects and traits influenced by genotypes result in the simultaneous evolution maternal effects have different evolutionary of the progeny environment (maternal effect) dynamics than “normal” traits (41, 43, 78). For and progeny adaptations to that environment. example, theoretical models (41, 43) have This accelerates the rate of coevolution demonstrated that maternal effects can result in between maternal traits and traits that affect time lags in response to natural selection and progeny fitness. can even result in short-term maladaptive Maternal effects can also create a conflict of responses to natural selection (i.e., a response interest between progeny and their parents. For in the opposite to expected direction). This is example, the size of egg that maximizes because progeny phenotypes are influenced by maternal fitness is generally different from the genes influenced in the maternal generation. egg size that will maximize progeny fitness We thus cannot partition evolution into the (because of fecundity selection on mothers), simple components of selection within resulting in selection on progeny for the ability generations and the response to selection across to manipulate the amount of resources allocated generations (78). The progeny environment is to each egg and selection on mothers for the in part genetically based (through the mother’s ability to prevent this manipulation. Parent- genotype) and can evolve through selection on offspring conflict has been extensively progeny. explored with regards to parental care (e.g., 35) Maternal traits that influence offspring and thus will not be discussed here. phenotypes also experience selection at the level of the family rather than just at the level The Ecological Significance of the individual, changing the dynamics of the of Maternal Effects selection response and changing the So far I have focused on the influence of equilibrium allele frequencies and maternal effects on evolutionary dynamics. heterozygosities expected to evolve at maternal Why should ecologists care about maternal effects loci (78). When a genotype affects both effects? There are numerous reasons. Many of the fitness of a mother and the fitness of her the phenotypes that influence ecological progeny in the same way (both positively or properties and population dynamics of negatively) the response to selection will be organisms are maternally controlled traits. For accelerated because the among-family example, recent theoretical research component of selection enhances the effect of demonstrates that population cycles of rodents selection at the individual level. Thus, and forest moths can be driven by maternal adaptation may be significantly influenced by effects (34, 60). Dispersal (and thus dispersion) selection occurring at levels other than the level in plants is generally influenced by fruit and of the individual, contrary to the widely seed-coat traits, both of which are maternally accepted understanding of adaptation. produced (7, 8). Niche-breadth is often determined by maternal oviposition decisions phenotype of their progeny (review in 25). rather than progeny feeding decisions Also, females that must oviposit on low quality (especially in herbivorous insects; 26, 57). larval substrates may produce larger progeny Dormancy of progeny (e.g., diapause), which than if they had encountered higher quality affects generation time and voltinism, is often oviposition substrates (e.g., 29). The ability of maternally controlled (5, 8; see below). females to manipulate the phenotype of their Maternal effects also provide a tool by progeny in response to environmental which females can adaptively manipulate the conditions provides an important mechanism phenotype of their progeny. In many organisms by which insect populations can adapt to living the maternal environment provides a reliable in a variable environment. indicator of the environmental conditions that their progeny will encounter (either biotic or Host Plant-Mediated Maternal Effects abiotic). In such cases, maternal effects may in Stator limbatus evolve as mechanisms for cross-generational Recent theoretical and empirical research phenotypic plasticity (also called “trans- thus indicates that maternal effects are common generation phenotypic plasticity”; 25, 50) in nature and that they can be evolutionarily whereby, in response to a predictive and ecologically very important (reviews in environmental cue (e.g. high or low host 51). One objective of this manuscript is to density, short or long photoperiod) a mother encourage ecologists to examine maternal can program a developmental switch in her effects in their own study system. This is offspring, or change her pattern of resource contrary to the perspective of many biologists allocation to those progeny in a manner up until recent times, which can be illustrated appropriate for the environmental conditions by a quote from Doug Falconer’s (10) classic predicted by the cue. In other words, females text in quantitative genetics. Falconer notes that can respond to predictive cues by changing the maternal effects are a “troublesome source of type of progeny that they produce to maximize environmental resemblance” that need to be progeny fitness (25). controlled for when doing genetic and Examples of cross-generational phenotypic evolutionary experiments. Until recently, most plasticity abound in insects (review in 25) and biologists shared this opinion. Maternal effects other organisms (e.g., plants; 8). For example, are considered in experiments because they can in many multivoltine species, females that be confounded with genetic effects, leading to encounter rapidly cooling temperatures or overestimation of genetic variances, and may decreasing day lengths produce offspring that even obscure the detection of genetic variances immediately enter diapause (a quiescent state) (67). Few researchers have examined maternal whereas females that encounter increasing day effects to understand their evolutionary and lengths or warming temperatures produce ecological significance. I will argue here that progeny that immediately start growth and simply controlling for maternal effects or, even development (5, 50). For insects using worse, ignoring maternal effects in our studies seasonal/ephemeral resources, environmental will ensure that we misunderstand the cues such as crowding, temperature, or mechanisms producing many of the patterns photoperiod may be predictable indicators of that we observe in nature. I will attempt to future deterioration of habitat quality and convince readers that maternal effects need to impending food shortage. In many species, the be considered in ecological studies because environment that females experience prior to they (a) influence responses to natural (or during) egg laying influences the flight selection, and (b) can respond to natural selection, providing an important mechanism paloverde (C. floridum) in the field produce for adaptation to variable environment (via progeny that performed better when reared on cross-generational phenotypic plasticity). this host in the lab than did progeny of To illustrate the importance of maternal populations of S. limbatus collected from seeds effects I am going to review recent work done of other species. This same result was obtained by myself and my colleagues on the biology of when they compared beetles reared from these the seed beetle, Stator limbatus (Coleoptera: same hosts within a single population; beetles Bruchidae). Like other seed beetles, the biology reared from blue paloverde produced progeny of S. limbatus revolves around seeds. Females that performed better on blue paloverde. David lay eggs directly onto the surface of their host proposed two explanations for this result. S. seeds. When these eggs hatch, larvae burrow limbatus populations may be genetically into the seed where they complete development differentiated (among populations) or and pupate. Larvae cannot move among seeds; genetically sub-structured (within populations), they are restricted to the seed that their mother such that some beetles are adapted to blue has chosen for them. They eventually emerge paloverde and other beetles are adapted to a from the seed as adults. Females take ≈ 1 to 2 d different host. Alternatively, these results may to mature and then begin mating and laying be produced by a host-plant mediated maternal eggs on seeds. S. limbatus is great for effect in which beetles reared from blue laboratory studies of insect life histories and paloverde produce progeny that are better able maternal effects because egg-to-adult to use this host, possibly because females turn development time is short (about 3 weeks at on genes in their progeny. The diet upon which 30° C), adult females can lay almost all of their mothers are reared has been shown to influence eggs within about 5 d post-emergence, and the phenotype of their progeny in a few other females do not need access to food or water as herbivorous insects (e.g., 36, 37, 45, 49, 58-60; an adult (they are facultatively aphagous; but see 76 for an exception) so we decided to providing access to food and water has very test this maternal effects hypothesis. little affect on the their life history). To test the maternal effects hypothesis, we Stator limbatus is a generalist seed-feeder (32) performed a simple experiment in which that is distributed throughout the southwestern beetles were reared in the lab for a couple United States and south into northern South generations on a common host (A. greggii) to America (38, 39) where it uses > 70 host plant remove environmental effects brought in from species in at least 9 genera. In central Arizona, the field, and then split beetles onto seeds of S. limbatus commonly uses seeds of two host two host plants, blue paloverde and catclaw plants, blue paloverde (Cercidium floridum) acacia. After one generation of rearing, we and catclaw acacia (Acacia greggii). These randomly mated all individuals in the species differ substantially in their suitability experiment (acacia-reared females mated to for larval development – beetles reared on acacia-reared males, acacia-reared females seeds of acacia have higher survivorship (>97% mated to paloverde-reared males, etc.), and vs. < 50%) and develop faster (mature sooner) split all progeny between acacia and paloverde than beetles reared on seeds of paloverde (21, seeds. As observed in previous studies, we 31, 32). found that paloverde seeds were a poor host for My interest in Stator was initially stimulated S. limbatus larvae, compared to catclaw acacia; by research published by David Siemens and egg-to-adult mortality was much higher (> 50% his collaborators (68-72). They demonstrated vs. < 5%), and development time is much that S. limbatus collected from seeds of blue longer (≈ 28 vs. ≈ 23 days) for larvae reared on (C. floridum) produce progeny that have higher Mothers reared onAcacia greggii survivorship, develop faster, and mature at a Mothers reared onCercidium floridum 3.4 larger body size than do progeny of mothers Female progeny M ale progeny 3.3 that were reared on acacia (A. greggii), and (2) 3.2 this effect in due to an environmentally-based 3.1 maternal effect – the father’s diet does not 3.0 affect the phenotype of his progeny. 2.9

Body Mass (mg) Mass Body 2.8 Maternal Effects Mediate Diet Expansion 2.7 in Stator limbatus AcaciaCercidium AcaciaCercidium One of my primary research interests is in Rearing Host of Progeny how insects shift among host plants or expand their diet to include new host plants. Figure 3 For Stator limbatus, the host upon which a Understanding the evolution of insect diet female parent is raised affects the size of her progeny breadths is of central importance to  whether they are reared on seeds of Acacia greggii understanding the evolution and diversification or Cercidium floridum, progeny are larger if their of insect-plant relationships, a key component mother was reared on C. floridum. The host upon in our broader attempt to understand species which a male parent is reared does not affect the size interactions and diversity. Unfortunately, most of his progeny (32). studies of insect diet evolution suffer from having limited information on the history of seeds of paloverde than for larvae reared on host use patterns; historical patterns can only seeds of acacia (21, 31). Most interestingly, we be inferred from modern patterns. However, observed a striking host-plant mediated recent introductions of non-native plants and maternal effect; mothers reared on paloverde the subsequent expansion of herbivores onto produced progeny that survived better, were these plants provide a powerful tool for larger at maturation and matured sooner than analyses of diet breadth evolution. progeny produced by mothers reared from S. limbatus has a very broad diet relative to acacia, regardless of the host on which the the diet of other species of Stator (38, 39, 53) progeny were reared (e.g., Fig. 3). The effect of or even other genera of bruchids. Despite its maternal host species on progeny survivorship extensive diet breadth, S. limbatus has never is probably due to natural selection occurring been found to use seeds of Texas ebony during the experiment; remember that mortality (Chloroleucon ebano; Fabaceae; Mimosoideae) is very high on paloverde seeds so that there is within the natural distribution of this plant intense natural selection for larvae that can (southern Texas and northern Mexico; 53). survive better on this species. However, we This is a particularly interesting observation cannot explain the effect of maternal diet on because Texas ebony is used as a host plant by progeny development time and body size at S. beali, the sister species to S. limbatus (53). maturation as a response to selection during the Recently, Texas ebony has been introduced as experiment – the host that fathers were reared an ornamental tree in the Phoenix metropolitan upon did not affect these traits in their progeny. area of Arizona (introduced post-1972; Phoenix Only the host that mothers were reared on Botanical Garden records). S. limbatus has mattered, indicating an environmentally-based since colonized this plant; adults readily maternal effect. oviposit on Texas ebony seeds in both nature The take-home messages from this first and the lab, and seeds of Texas ebony experiment: (1) females reared on paloverde successfully produce reproductively mature S. populations, including the population that uses limbatus adults in nature. In the field, egg-to- Texas ebony. You'll remember that in previous adult survivorship averages > 10% in the sites field work we had found that survivorship on that I have examined (26). Texas ebony seeds is generally >10% in the In a series of experiments (26, 28) my field (26). Why this discrepancy? We expected colleagues and I examined two features of the survivorship to be higher in a controlled, ecology and evolution of this expansion by S. parasite-free lab environment. limbatus onto Texas ebony. First, is there pre- To answer this question we must consider existing variation in the ability to survive on the conditions under which S. limbatus Texas ebony within populations of S. limbatus populations were maintained in the lab. To that are not associated with this host? Such control for host-associated maternal effects we variation, if genetic, provides the raw material had raised each of our populations on A. for adaptation to this host once it has been greggii for one generation prior to the colonized by adults. Second, have populations experiment. However, in nature beetles in of S. limbatus that are using Texas ebony in Papago Park are colonizing Texas ebony from central Arizona begun to adapt to this host in blue paloverde, C. floridum (there is no A. the short time since its introduction? As you'll greggii in the vicinity). We know from see shortly, this study evolved into an previous experiments that larvae produced by examination of how maternal effects, mothers that had been reared on C. floridum are stimulated by the parental host plant, influence different from those produced by mothers the ability of progeny to survive on Texas reared on A. greggii. Maybe rearing S. limbatus ebony. on A. greggii (instead of C. floridum) for a To address the two questions asked above, single generation in the lab can account for the we performed a simple experiment in which we difference in survivorship on Texas ebony (a) collected beetles from four populations in between lab and field populations. To test this nature (one in northern Texas where there is no hypothesis, we performed an experiment in Texas ebony, two in central Arizona where which we reared beetles for one generation on ornamental Texas ebony is uncommon or not seeds of either A. greggii, C. floridum, or Texas present, and one population in Papago Park in ebony, and then reared progeny of these beetles Phoenix where beetles use ornamental Texas on seeds of Texas ebony. As expected the host ebony), (b) raised these beetles in the lab for at that parents were reared upon influenced the least one generation on seeds of A. greggii (to survivorship of their progeny. When parents remove maternal effects associated with the were reared on A. greggii, survivorship of hosts that beetles were collected from in progeny on Texas ebony was about 3% (Fig. nature), and then reared all populations for one 4b), exactly as seen in the previous experiment generation on seeds of Texas ebony. We found (Fig. 4a). When parents were reared on Texas that although egg-to-adult survivorship on ebony, survivorship of progeny on this host seeds of Texas ebony varied among families (a increased a bit, to between 4 and 8 %, as would prerequisite for adaptation to be possible), there be expected if high mortality during the was no evidence that a population using this parental generation resulted in some adaptation host in nature (Papago Park population) had to this host in the lab. Most interestingly, begun to adapt to it (Fig 4a). However, the however, was the result that when parents were most interesting observation from this reared on seeds of paloverde (C. floridum) the experiment was that larval survivorship on survivorship of their progeny on Texas ebony Texas ebony was less than 4% in all Survivorship of Stator limbatus larvae on 6 Figure 4 N = 82N = 155 N = 98 N = 110 seeds of Texas ebony (Chloroleucon ebano). (a) 5 Comparison among populations of S. limbatus; the Papago Park population was collected from Texas 4 ebony in nature; (b) Parents reared on C. floridum or Texas ebony produce progeny that have higher 3 survivorship on Texas ebony (the three color bars represent three replicates of the experiment); (c) One 2 generation of rearing on seeds of A. greggii nullifies treatment differences, indicating that the parental host Survivorship (%) 1 effect in non-genetic (the two color bars are 0 replicates). Data from 26. Papago Scottsdale Apache Van Horn Park Junction experiments (previous section of this Population manuscript). However, it is also possible that, 25 because beetles experience high mortality when reared on paloverde (generally >50%; 20 discussed earlier), evolution (genetically-based change) may occur in the lines reared on 15 paloverde, and adaptation to paloverde may result in simultaneous adaptation to Texas 10 ebony (due to genetic correlations across environments; 77). We thus need to 5

Survivorship (%) experimentally demonstrate that this parental 0 host effect is an environmentally-based A. greggii C. ebano C. floridum maternal effect rather than a genetically-based Maternal Host response to natural selection during the experiment. To do this we reared beetles on 6 Selected on Acacia greggii seeds of either paloverde or acacia for multiple Selected on Cercidium floridum 5 generations and then asked whether the two types of lines had begun to differentiate in their 4 ability to survive on Texas ebony. Our first 3 group of lines was reared on seeds of paloverde for four generations; if evolution in response to 2 paloverde could occur in a single generation in 1 our earlier experiment, then a fair bit of Survivorship (%) evolution should occur over four generations. 0 For comparison, we reared another set of lines Scottsdale Apache J Mixed continuously on seeds of acacia, with no access Population to seeds of paloverde. At the end of our short natural selection experiment, we reared all increased to >11%, matching the survivorship beetles on seeds of acacia for a single observed in the field on this host. generation, and then scored survivorship of Rearing parents on paloverde most likely larvae on seeds of Texas ebony. The logical affects the survivorship of their progeny on basis for this experiment is as follows; if Texas ebony due to a environmentally-based observed effects of parental rearing on maternal effect, as seen in our first set of paloverde represent genetic responses to selection, then genetic differences should our previous experiments females encountered develop between the paloverde and acacia lines their rearing host immediately after emerging during the experiment, and these differences from a seed, but were quickly transferred to should persist in the population when the their test host. Thus, the post-emergence beetles are reared for a single generation on experiences of females differed among seeds of acacia. However, if observed effects of treatments, but only for a short period of time. parental rearing on paloverde represent non- We should thus only expect a small difference genetic effects of parental environment, then a in survivorship among treatments in the single generation of rearing on a common host previous experiments, relative to the effects species should reduce or even eliminate these observed in this last experiment. differences. This latter possibility is what we in These results have interesting implications fact observed (Fig. 4c); the two types of lines for the ecology of S. limbatus. Remember that did not differ in larval survivorship on seeds of S. limbatus does not use Texas ebony as a host Texas ebony, and survivorship of all lines was anywhere that the beetle and tree are naturally <4%, as was observed when parents were sympatric. Our results suggest that they may reared on acacia in each previous experiment not use Texas ebony in these areas because (Figs. 4a and 4b). there is no paloverde present to facilitate the So far these results indicate that maternal diet expansion (Texas ebony is also grown as rearing host affects the ability of progeny to an ornamental tree in parts of southern Texas survive on Texas ebony. But is it really but these trees are not used by S. limbatus maternal diet that influences performance of indicating that colonization of Texas ebony in her progeny? In 1997 we (28) performed a Arizona is not the result of differences between simple experiment in which we exposed naturally occurring and ornamental trees). females to seeds of either the native blue More generally, our results indicate that paloverde or the non-native Texas ebony while whether insects incorporate non-native plants these females were maturing their eggs (within into their diet will depend in part on the species 12 h after emerging as an adult). We then composition of the local plant community and forced these females to lay eggs on Texas that changes in the plant community may ebony. Females had all been reared on seeds of facilitate shifts between host species by A. greggii, so the two treatments differed only herbivorous or parasitic insects. For example, in the seed species that they encountered during introducing paloverde into southern Texas may egg maturation. Also, females cannot feed facilitate the expansion of S. limbatus onto externally on dried seeds, so the two treatments Texas ebony. Our results also indicate that are nutritionally identical. When females patterns of host use by insects in one locality matured eggs in contact with seeds of blue may not adequately predict whether plants will paloverde, nearly 50% of their progeny be colonized by insects if they are introduced to survived from egg-to-adult, compared to only another locality, nor the hosts that insects will about 5% survivorship for progeny of mothers colonize when the insects are introduced to a that had never encountered seeds of paloverde! new locality (e.g., as a biocontrol agent). For S. This is a substantially larger treatment effect limbatus, host use in southern Texas does not than we observed in any previous experiments. predict host use in central Arizona because Why? I interpret this result as indicating that it interactions between the insect and its hosts are is not female diet that affects the survivorship influenced by community composition. of their progeny, but instead it is female Interactions such as these may explain why experience after they emerge from a seed. In many introduced biological control agents 8 before we can understand the mechanism by N = 20 trees 7 which female encounters with host seeds 6 influences the survivorship of their progeny, 5 we must spend a moment discussing some 4 basic concepts concerning the evolution of egg 3 size. Mathematical analyses of optimal egg size 2

Number of Trees are largely based on the simple but illuminating 1 framework initially established by Smith and 0 -0.4 -0.2 0.0 0.2 0.4 0.6 0.8 to -0.2 to 0.0 to 0.2 to 0.4 to 0.6 to 0.8 to 1.0 Fretwell (73). They noted that the number of Selection Intensity (i) grand-progeny a female will produce depends on both the number of progeny that she produces and the fitness of those progeny. They 1.0 r = 0.69 started with two basic assumptions; progeny P < 0.001 fitness increases with increasing parental 0.5 investment per offspring (e.g., egg size) and for any fixed amount of parental investment into 0.0 reproduction there is a trade-off between the size of progeny that a female can make and the number of progeny that she can make. Thus,

Selection Intensity (i) -0.5 selection favors larger progeny because larger 0.00 0.20 0.40 0.60 0.80 1.00 progeny have higher fitness and thus produce Seed-coat Resistance (Mean per tree) more grand-progeny, but selection also favors Figure 5 (a) The intensity of natural selection on making smaller progeny because then females Stator limbatus egg size in the field varies among can make more progeny and thus produce more individual Cercidium floridum trees (data for selection grand-progeny. Egg size is thus under on egg length within the Scottsdale population of S. balancing selection, with some intermediate limbatus). (b) This variation in selection correlates value of egg size maximizing maternal fitness with the degree to which seeds are resistant to larvae. (note, however, that the size of egg that maximizes offspring fitness is necessarily unexpectedly attack non-target species (44) and larger than the size that maximizes maternal why plants may be attacked by insects in one fitness, creating a conflict between mothers and locality but not another. Thus maternal effects their offspring). This simple model also can have a previously unrecognized role in demonstrates that any environmental variable influencing species interactions within that affects the relationship between egg size communities and we should consider these and progeny fitness can result in a change in maternal effects when predicting the ecological the optimal egg size. For example, as the and evolutionary consequences of changing difference in survivorship between larvae species distributions. hatching from small vs. large eggs increases, the optimal egg size will shift toward a larger Egg Size Plasticity: An Adaptive value and we would expect larger eggs to Maternal Effect evolve in our population. What are females doing to their progeny For S. limbatus, the fitness consequences of that influences the survivorship of larvae on variation in egg size differ substantially among seeds of Texas ebony? The answer involves tree species and among individual trees within changes in egg size and composition. However, poorly defended seeds, resulting in weak or 1.00 even no selection favoring large eggs (Fig. 5b). For our purposes here, though, variation in 0.80 selection on S. limbatus egg size among species 0.60 of trees is of more interest. Mortality of larva is generally > 50% on seeds of C. floridum. Most 0.40 of this mortality occurs as larvae attempt to 0.20 penetrate the seed coat (due to chemical Cercidium floridum defenses on the seed coats; M. E. Czesak & C. 0.00 0.38 0.40 0.42 0.44 0.46 0.48 0.50 W. Fox, unpublished data). Because larvae Survivorship (Egg-to-Adult) hatching from larger eggs are better able to Egg Width penetrate C. floridum seed coats, we observe strong directional selection for large eggs when eggs are laid on this host (averaged across all 1.00 trees in a population; Fig. 6a). On seeds of A. 0.80 greggii and a different paloverde species, C. microphyllum (small-leaf paloverde, a host 0.60 species that we have not yet discussed in this 0.40 paper), larval mortality is quite low (generally < 3% on A. greggii and < 25 % on C. 0.20 microphyllum) and there is little or no selection Acacia greggii favoring large eggs on these hosts (Fig. 6b); 0.00 0.38 0.40 0.42 0.44 0.46 0.48 0.50 progeny hatching from small eggs survive Survivorship (Egg-to-Adult) about as well as progeny hatching from large Egg Width (mm) eggs. Thus, selection strongly favors progeny Figure 6 The relationship between the size of eggs hatching from large eggs when females laid by a female Stator limbatus and the egg-to-adult oviposit on seeds of C. floridum, but, because survivorship of her larvae on seeds of (a) Acacia progeny hatching from small eggs perform well greggii and (b) Cercidium floridum. Data are for the on A. greggii or C. microphyllum, selection Scottsdale population in 24. favors females that lay smaller eggs on these species. In general, the harsher the environment hosts because they will have higher fecundity for progeny (and thus the higher the larval (due to the previously discussed trade-off mortality) the greater the difference in between egg size and fecundity). survivorship between progeny hatching from Based on this difference in selection among large vs. small eggs, and thus the greater the hosts we would expect populations of S. magnitude of selection favoring larger eggs. limbatus collected from C. floridum (upon For example, selection intensities vary between which selection favors larger eggs) to evolve i ≈ -0.4 to i ≈ 1.0 among individual trees within larger eggs than populations collected from A. a single population of blue paloverde (C. greggii or C. microphyllum. This is exactly floridum; Fig. 5a). This variation appears to what we have observed (24; C. W. Fox result from variation in chemical defenses unpublished data). However, many populations among trees; beetles experience high mortality of S. limbatus have access to both C. floridum on seeds of well-defended trees, resulting in and one of the two host species upon which substantial selection favoring large eggs, but selection favors small eggs (either A. greggii or experience relatively low mortality on seeds of C. microphyllum). This results in disruptive Eggs on Cerci di um fl ori dum C. floridum to A. greggi i Eggs on Acaci a greggi i 0.50 A. greggi i to C. floridum 0.028 0.47 0.026 0.44 0.023 0.41 0.021 0.38 E gg Width (mm) E gg Width

E gg Mass(mg) 0.018 0.35 2.0 2.3 2.6 2.9 3.2 3.5 3.8 4.1 0.016 0 122436486072 Fe male M as s (mg) Hours

60 1.00 50 0.80 40 0.60 30 20 0.40 10 0.20 Lifetime Fecundity Lifetime 0 0.00 2.0 2.4 2.8 3.3 3.7 4.1 0.025 0.027 0.029 0.031 0.033 0.035 E gg-to-adult Sur vivor s hip Fe male M as s (mg) E gg Mass (mg)

Figure 7 Egg size plasticity in Stator limbatus. (a) Females lay larger eggs on Cercidium floridum than on either Acacia greggii (shown) or C. microphyllum (data are for the Apache Junction population from 29); (b) Females have lower fecundity of C. floridum; (c) When switched between host plants, females switch the size of eggs that they lay (unpublished data; the asymmetrical response originally published in 29 was not repeatable and so is not presented here); (d) Females that mature eggs on C. floridum lay larger eggs on Texas ebony, which affects the survivorship of their progeny (data from 28). selection within the beetle population, with regions where C. floridum is sympatric with at selection variably favoring large eggs (when a least one of the other two hosts, we find larger female encounters C. floridum) or small eggs eggs on C. floridum than on either of the other (when they encounter A. greggii or C. two hosts, suggesting that either some degree microphyllum). This type of disruptive of population substructure has evolved in these selection can have interesting evolutionary populations, or that females are capable of implications; it can maintain genetic variation producing different size eggs in response to the in a population (by simultaneously favoring different host plants (i.e., plasticity in egg size). multiple extreme phenotypes; 33), can result in To test the hypothesis that females exhibit population sub-structuring (a prerequisite to egg size plasticity in response to their host sympatric speciation; 6), and can lead to the species, we collected beetles from the field, evolution of phenotypic plasticity (77). reared them in the lab on a common host (A. Interestingly, if we collect S. limbatus eggs greggii) for at least one generation, and then from seeds of these three host species in exposed females to seeds of either C. floridum or A. greggii. When females were forced to approximately 6-12 h on C. floridum relative to oviposit on seeds of C. floridum they laid laying on A. greggii. However, paired substantially larger eggs than did females oviposition preference tests indicate that, exposed to A. greggii (Fig. 7a; note that the Y- despite high larval mortality, females either axis in the figure is egg width; egg mass differs prefer to oviposit on C. floridum (when by >25% between the treatments; 29) (see 25 compared with A. greggii), or show no and 30 for comparable data for the comparison preference for either host (31). Also, when between C. floridum and C. microphyllum). deprived of hosts during egg maturation, and Females are capable of adjusting egg size in thus forced to retain eggs longer, first-laid eggs response to the host upon which they lay eggs are small (i.e. the size they normally lay on A. because they delay oviposition for at least 24 h greggii) regardless of the host upon which eggs after emergence, during which time they finish are laid. When females are forced to lay on maturing eggs. If they are in contact with their other non-preferred hosts (or non-hosts), on oviposition substrate (seed) during egg which egg-laying is also delayed, they also lay maturation they know upon which host their small, Acacia-size eggs (C. W. Fox, progeny will develop, and have the opportunity unpublished data). Thus, it appears that the for facultative responses to the host species. delay in oviposition on seeds of C. floridum is a Females take advantage of this to manipulate consequence of laying larger eggs on this host the phenotype of their offspring (i.e., they and not the cause of the difference in egg size exhibit a maternal effect) by laying large eggs between hosts. on C. floridum (where progeny hatching from When female S. limbatus are forced to large eggs have a substantial fitness advantage) switch among host species in the laboratory and laying small eggs on A. greggii or C. (from A. greggii to C. floridum or from C. microphyllum. However, laying large eggs on floridum to A. greggii) they shift the size of C. floridum comes at a fecundity cost to eggs that they lay (Fig. 7c), but the switch females − they lay substantially fewer eggs on doesn't begin until approximately 24 h after C. floridum than on either A. greggii or C. exposure to the new host. We took advantage microphyllum (Fig. 7b) due to a trade-off of this observation to test whether egg size between egg size and egg number. A trade-off plasticity in S. limbatus is adaptive; we between egg size and egg number is also conditioned females to lay large eggs evident within treatments (hosts); there is a (conditioned on C. floridum) or small eggs negative correlation between egg size and egg (conditioned on A. greggii), and then forced all number, after controlling for body size, on each females to oviposit for 24 h on seeds of C. host (29). floridum. Eggs from the A. greggii-conditioned Egg size plasticity in S. limbatus is not the females subsequently had very low egg-to- result of female reluctance to lay eggs on C. adult survivorship on C. floridum (< 1%), while floridum. Because larval survivorship is very eggs laid by females that were conditioned on low on C. floridum we might expect females to C. floridum had substantially higher egg-to- evolve avoidance of this host in preference for adult survivorship on this host (24%). This A. greggii or C. microphyllum (on which larval demonstrates that females that fail to exhibit survivorship is high). Such reluctance to egg size plasticity in response to C. floridum oviposit would result in prolonged egg will have very low fitness (because all of their retention when encountering C. floridum, and progeny will die) compared to females that thus possibly increased resource allocation to switch to laying larger eggs on this host. these eggs. Females do in fact delay egg-laying Mechanistic biology of seed-coat resistance seeds are uncorrelated among trees, indicating and egg size plasticity  So females respond that they must be influenced by different traits to the host upon which they will lay eggs by of the seeds (30). shifting egg size in a manner consistent with Does egg size plasticity have anything to do our understanding of natural selection on egg with the ability of S. limbatus larvae to use size. Why do progeny hatching from large eggs seeds of Texas ebony? In our earlier have a fitness advantage over progeny hatching experiment when we exposed females to seeds from small eggs when reared on seeds of C. of either the native blue paloverde or the non- floridum? What cues are females responding native Texas ebony while these females were to? How does this influence survivorship of maturing their eggs, and then forced these larvae on the exotic host, Texas ebony? At this females to lay eggs on Texas ebony, we found time, we cannot answer these questions, but we that progeny of paloverde-exposed females had can begin to make some educated guesses. substantially higher survivorship on seeds of The primary cause of mortality of S. Texas ebony than did progeny of mothers that limbatus larvae on seeds of C. floridum appears had never experienced paloverde seeds. When to be chemical defenses upon the seeds; we measure eggs in these treatments we find extractions from C. floridum seeds cause that paloverde-exposed females laid larger eggs mortality of larvae when precipitated onto than females that had never encountered seeds of C. microphyllum or A. greggii (70; M. paloverde, and that egg size correlated E. Czesak & C. W. Fox, unpublished data). It is positively with larval survivorship within each not yet known what chemicals result in larval treatment (Fig. 7d), suggesting that the mortality, but it is clear that these chemicals are difference in larval survivorship between different from the cues that females respond to treatments is due at least in part to plasticity in when deciding what size egg to lay. We have egg size. However, plasticity in egg size is only two kinds of evidence demonstrating this. First, part of the explanation. In the range of egg females do not respond behaviorally to seed sizes that overlap between the two treatments, coat extractions that kill larvae when survivorship of progeny of paloverde-exposed precipitated onto seeds of other hosts. Second, mothers is still substantially higher than the we have examined S. limbatus egg size and survivorship of progeny of Texas ebony- larval mortality in a paloverde hybrid swarm in exposed mothers, indicating that eggs also eastern California (USA) where C. floridum differ between treatments in their composition and C. microphyllum hybridize and backcross or gene expression. Unfortunately, we do not (40, 72). Hybrid trees vary substantially in how yet understand how eggs differ in composition. well defended their seeds are against larvae of S. limbatus, ranging from well defended (< 25 The Evolutionary Genetics % of larvae successfully penetrate the seed of Egg Size Plasticity coat) to almost completely undefended (nearly The most recent focus of my laboratory has 100% of larvae successfully penetrate the seed been on the evolutionary genetics of this egg coat; Fox et al. 1997c). Hybrid trees also vary size plasticity. For a trait to continue to evolve in whether females recognize them as a C. in nature, there must be genetic variation floridum (and lay large eggs on their seeds) or present within populations. For two traits to recognize them as a C. microphyllum (and lay differentiate from each other, the genetic smaller eggs on their seeds). However, the correlation between them must be < 1.0. In this degree to which seeds are resistant to beetles case, we can treat the size of eggs that females and the size of eggs that females lay on these lay on C. floridum and the size of eggs that they lay on A. greggii as two different traits. these two hosts can diverge and that egg size For egg size to evolve it must be heritable (i.e., plasticity is thus capable of evolving in the variation among individuals must in part be response to natural selection. caused by genetic differences among We have since been expanding our genetic individuals). For egg sizes to evolve separately analyses to include examination of the genetic on these two hosts (smaller eggs on A. greggii correlation between egg size and fecundity, the and larger eggs on C. floridum) then the genetic influence of male parental investment (a correlation between them must be < 1.0; a paternal effect) on egg size and female genetic correlation of 1.0 indicates that fecundity, and covariation between egg size selection for a change in egg size on one host and other phenotypic traits. Also, as I write this will result in exactly the same change on the chapter, we are in the midst of an artificial other host, preventing egg sizes from further selection experiment in which we are creating diverging on the two hosts. populations of beetles that lay either larger or We can quantify these genetic variances and smaller eggs on C. floridum and A. greggii to genetic correlations using a standard test hypotheses concerning the evolution of quantitative genetic technique called a half-sib genetic correlations between traits and to breeding design. In this design, we mate each examine the genetic basis of the selection of a random selection of males in our study to responses. multiple females (in this study, each male was mated to four females) creating a population of The Take-home Message progeny that is composed of full-sibs (share the Stator limbatus is a widely distributed seed same mother and father), half-sibs (share beetle that uses many host species throughout fathers but not mothers) and unrelated it’s broad distribution. These host species vary individuals. We then raise these progeny and substantial in their suitability for larval collect data on egg size and other traits of development. However, females have interest from every individual. The strength of information on what hosts their progeny will this half-sib design is that it allows us to tease develop upon before they lay eggs, allowing apart additive genetic variances and them the opportunity to manipulate the covariances (the kind that influence responses phenotype of their progeny in a manner likely to natural selection) from other sources of to increase progeny fitness in each variance and covariance that result in similarity environment. In part females manipulate among individuals within a family (including progeny phenotype (and fitness) by changing some types of genetic and non-genetic the size of eggs that they lay (laying larger eggs variances). We found that genetic variation is on the better defended host species) and in part present within populations for the size of eggs they manipulate progeny phenotype by laid on seeds of both A. greggii and C. floridum manipulating egg composition (28). (the heritability, h2, ranged between 0.217 and Thus, maternal effects are an essential 0.908), and that the heritability of egg size component of the biology of S. limbatus. They differed between populations and was higher appear to have evolved as an adaptation for on A. greggii than on C. floridum (18). We also dealing with a variable environment (variation found that the evolution of egg size plasticity is among hosts in suitability). Also, females are in part constrained by a high genetic correlation genetically variable in their expression of the across host plants (rG > 0.6). However, the maternal effect so that the maternal effect may cross-environment genetic correlation is less still be evolving within populations. Yet, than 1.0, indicating that the size of eggs laid on despite the fact that we know more about the significance of maternal effects for the biology University of South Carolina) and a NSF of S. limbatus than for most other organisms postdoctoral fellowship (DEB 94-03244) to (but see 51 for other examples of well studied Charles Fox. systems) we really know very little about this system. Do females respond to other host References species (we have only examined three species)? 1. Bernardo J. 1996. The particular maternal How does variation in the relative abundance effect of propagule size, especially egg size: of host species influence the evolutionary and patterns, models, quality of evidence and ecological dynamics of egg size and egg size interpretations. American Zoologist 36: plasticity? How does egg size plasticity 216-236. influence other ecological interactions, such as 2. Boersma M. 1997. Offspring size and larval competition between beetle species, and parental fitness in Daphnia magna. how do these interactions influence the Evolutionary Ecology 11: 439-450. evolution of egg size and egg size plasticity? 3. Boggs CL. 1990. A general model of the What constraints are there on the evolution of role of male-donated nutrients in female egg size plasticity? The list of questions yet to insects' reproduction. The American be asked and answered is long. Naturalist 136: 598-617. Most ecologists and entomologists give 4. Chen PS. 1984. The functional morphology little thought to maternal effects. Some design and biochemistry of insect male accessory their experiments in a manner that allows them glands and their secretions. Annual Review to remove maternal effects from their genetic of Entomology 29: 233-255. analyses, allowing them to better estimate 5. Danks HV. 1987. Insect Dormancy: An genetic variances and covariances for the traits Ecological Perspective. Biological Survey of interest (discussion in 67). Others simply of Canada Monograph Series no. 1, Ottawa, ignore maternal effects. The primary objective Canada. of this review was to use examples from my 6. Diehl SR, Bush GL. 1989. The role of own research on seed beetles to illustrate how habitat preference in adaptation and understanding maternal effects can be essential speciation. pp. 345-365 in Otte D & Endler to understanding ecological interactions in JA (eds.) Speciation and its consequences. nature. Of one thing we can be sure; future Sinauer Associates, Inc. Sunderland, MA, research on maternal effects promises to hold USA. great explanatory power for understanding the 7. Donohue, K. 1998. Maternal determinants evolution of life cycles and adaptation to of seed dispersal in Cakile edentula: fruit, spatially and temporally variable environments. plant and site traits. Ecology 79: 2771-2788. 8. Donohue K, Schmitt K. 1998. Maternal Acknowledgements environmental effects in plants: Adaptive I thank M.E. Czesak, K. Donohue, B. Pass, plasticity? pp. 137-158 in Mousseau TA, and C. Rauter for helpful comments on this Fox CW (eds.) Maternal Effects as manuscript. I also thank all of my collaborators Adaptations. Oxford University Press, New over the last few years, without whom much of York, USA. this work would not have been possible. 9. Dussourd DE, Ubik K, Harvis C, Resch J, Research discussed in this manuscript has been Meinwald J, Eisner T. 1988. Biparental funded by NSF DEB grant nos. 98-07315 and defensive endowment of eggs with acquired 99-96371 (to Charles Fox), USDA/CSRS grant plant alkaloid in the moth Utethesia no. 93-01887 (to Timothy Mousseau at the ornatrix. Proceedings of the National Environmental Entomology 28: 217-223. Academy of Sciences USA 85: 5992-5996. 20. Fox CW, Dingle H. 1994. Dietary mediation 10. Falconer DS. 1989. Introduction to of maternal age effects on offspring quantitative genetics. 2nd edition. Longman performance in a seed beetle (Coleoptera: Scientific, NY, USA. Bruchidae). Functional Ecology 8: 600-606. 11. Fox CW. 1993. The influence of maternal 21. Fox CW, Harbin AD, Mousseau TA. 1996. age and mating frequency on egg size and Suitability of a non-host palo verde for offspring performance in Callosobruchus development of Stator limbatus (Coleoptera; maculatus (Coleoptera: Bruchidae). Bruchidae) larvae. The Pan-Pacific Oecologia 96: 139-146. Entomologist 72: 31-36. 12. Fox CW. 1993. Multiple mating, lifetime 22. Fox CW, Martin JD, Thakar MS, Mousseau fecundity and female mortality of the TA. 1996. Clutch size manipulations in two bruchid beetle Callosobruchus maculatus seed beetles: consequences for progeny (Coleoptera: Bruchidae). Functional fitness. Oecologia 108: 88-94. Ecology 7: 203-208. 23. Fox CW, Mousseau TA. 1995. 13. Fox CW. 1994. The influence of egg size on Determinants of clutch size and seed offspring performance in the seed beetle, preference in a seed beetle, Stator beali Callosobruchus maculatus. Oikos 71: 321- (Coleoptera: Bruchidae). Environmental 325. Entomology 24: 1557-1561. 14. Fox CW. 1994. Maternal and genetic 24. Fox CW, Mousseau TA. 1996. Larval host influences on egg size and larval plant affects the fitness consequences of egg performance in a seed beetle: size in the seed beetle Stator limbatus. Multigenerational transmission of a Oecologia 107: 541-548. maternal effect? Heredity 73: 509-517. 25. Fox CW, Mousseau TA. 1998. Maternal 15. Fox CW. 1997. The ecology of body size in effects as adaptations for transgenerational a seed beetle, Stator limbatus: Persistence of phenotypic plasticity in insects. pp. 159-177 environmental variation across generations? in Mousseau TA, Fox CW (eds.) Maternal Evolution 51: 1005-1010. Effects as Adaptations. Oxford University 16. Fox CW. 1997. Egg size manipulations in Press, New York, USA. the seed beetle, Stator limbatus: 26. Fox CW, Nilsson JA, Mousseau TA. 1997. consequences for progeny growth. The The ecology of diet expansion in a seed- Canadian Journal of Zoology 75: 1465- feeding beetle - pre-existing variation, rapid 1473. adaptation and maternal effects? 17. Fox CW, Czesak ME. 2000. Evolutionary Evolutionary Ecology 11: 183-194. ecology of progeny size in arthropods. 27. Fox CW, Savalli UM. 1998. Inheritance of Annual Review of Entomology in press. environmental variation in body size: 18. Fox CW, Czesak ME, Mousseau TA, Roff Superparasitism of seeds affects progeny DA. 1999. The evolutionary genetics of an and grandprogeny body size via a non- adaptive maternal effect: Egg size plasticity genetic maternal effect. Evolution 52: 172- in a seed beetle. Evolution 53: 552-560. 182. 19. Fox CW, Czesak ME, Savalli UM. 1999. 28. Fox CW, Savalli UM. 2000. Maternal Environmentally-based maternal effects on effects mediate host expansion in a seed- development time in the seed beetle, Stator feeding beetle. Ecology in press. pruininus (Coleoptera: Bruchidae): 29. Fox CW, Thakar MS, Mousseau TA. 1997. Consequences of larval density. Egg size plasticity in a seed beetle: An adaptive maternal effect. The American Coleoptera: Bruchidae) en Sudamerica. Naturalist 149: 149-163. Opera Lilloana 37: 1-105. 30. Fox CW, Waddell KJ, des Lauriers J, 40. Jones CE. 1978. Pollinator constancy as a Mousseau TA. 1997. Seed beetle pre-pollination isolating mechanism survivorship, growth and egg size plasticity between sympatric species of Cercidium. in a paloverde hybrid zone. Ecological Evolution 32: 189-198. Entomology 22: 416-424. 41. Kirkpatrick M, Lande R. 1989. The 31. Fox CW, Waddell KJ, Mousseau TA. 1994. evolution of maternal characters. Evolution Host-associated fitness variation in a seed 43: 485-503. beetle (Coleoptera: Bruchidae): Evidence 42. Lacey EP. 1998. What is an adaptive for local adaptation to a poor quality host. environmentally induced parental effect? Oecologia 99: 329-336. pp. 54-66 in Mousseau TA, Fox CW (eds.) 32. Fox CW, Waddell KJ, Mousseau TA. 1995. Maternal Effects as Adaptations. Oxford Parental host plant affects offspring life University Press, New York, USA. histories in a seed beetle. Ecology 76: 402- 43. Lande R, Kirkpatrick M. 1990. Selection 411. response in traits with maternal inheritance. 33. Futuyma DJ. 1998. Evolutionary Biology. Genetical Research 55: 189-197. 3rd Edition. Sinauer Associates, Inc. 44. Louda SM, Kendall D, Connor J, Simberloff Sunderland, MA, USA. D. 1997. Ecological effects of an insect 34. Ginzburg LR. 1998. Inertial growth: introduced for the biological control of Population dynamics based on maternal weeds. Science 277: 1088-1090. effects. pp. 42-53 in Mousseau TA, Fox CW 45. McCauley GW Jr., Margolies DC, Resse JC. (eds.) Maternal Effects as Adaptations. 1990. Feeding behavior, fecundity and Oxford University Press, New York, USA. weight of sorghum- and corn-reared 35. Godfray HCJ. 1995. Evolutionary theory of greenbugs on corn. Entomologica parent-offspring conflict. Nature 376: 133- Experimentalis et Applicata 55: 183-190. 138. 46. Messina FJ. 1991. Life-history variation in a 36. Gould F. 1988. Stress specificity of seed beetle: adult egg-laying vs. larval maternal effects in Heliothis virescens competitive ability. Oecologia 85: 447-455. (Boddie) (Lepidoptera: Noctuidae) larvae. 47. Messina FJ. 1998. Maternal influences on Memoirs of the Entomological Society of larval competition in insects. pp. 227-243 in Canada 146: 191-197. Mousseau TA, Fox CW (eds.) Maternal 37. Haukioja E, Neuvonen S. 1987. Insect Effects as Adaptations. Oxford University population dynamics and induction of plant Press, New York, USA. resistance: the test of hypotheses. pp. 411- 48. Messina FJ, Mitchell R. 1989. Intraspecific 432 in Barbosa P, Schulz JC (eds.) Insect variation in the egg-spacing behavior of the Outbreaks. Academic Press, New York, seed beetle Callosobruchus maculatus. New York. Journal of Insect Behavior 2: 727-742. 38. Johnson CD, Kingsolver JM. 1976. 49. Morris RF. 1967. Influence of parental food Systematics of Stator of North and Central quality on the survival of Hyphantria cunea. America (Coleoptera: Bruchidae). USDA Canadian Entomologist 99: 24-33. Technical Bulletin 1537: 1-101. 50. Mousseau TA, Dingle H. 1991. Maternal 39. Johnson CD, Kingsolver JM, Teran AL. effects in insect life histories. Annual 1989. Sistematica del genero Stator (Insecta: Review of Entomology 36: 511-534. 51. Mousseau TA, Fox CW (eds). 1998a. Maternal Effects as Adaptations. Oxford 112-134 in Mousseau TA, Fox CW (eds.) University Press, New York, NY, USA. 375 Maternal Effects as Adaptations. Oxford pages. University Press, New York, USA. 52. Mousseau TA, Fox CW. 1998b. The 63. Savalli UM, Fox CW. 1998. Genetic adaptive significance of maternal effects. variation in paternal investment in a seed Trends in Ecology and Evolution 13: 403- beetle. Animal Behaviour 56: 953-961. 407. 64. Savalli UM, Fox CW. 1998. Sexual 53. Nilsson JA, Johnson CD. 1993. Laboratory selection and the fitness consequences of hybridization of Stator beali and S. male body size in the seed beetle, Stator limbatus, with new host records for S. limbatus. Animal Behaviour 55: 473-483. limbatus and Mimosestes amicus 65. Savalli UM, Fox CW. 1999. Effect of male (Coleoptera: Bruchidae). Southwestern mating history on paternal investment, Naturalist 38: 385-387. fecundity, and female remating in the seed 54. Parsons PA. 1964. Parental age and the beetle Callosobruchus maculatus. offspring. Quarterly Review of Biology 39: Functional Ecology 13: 169-177. 258-275. 66. Savalli UM, Fox CW. 1999. The effects of 55. Roach DA, Wulff R. 1987. Maternal effects male size, age, and mating behavior on in plants: evidence and ecological and sexual selection in the seed beetle evolutionary significance. Annual Review Callosobruchus maculatus. Ecology, of Ecology and Systematics 18: 209-235. Ethology and Evolution 11: 49-60. 56. Roff DA. 1997. Evolutionary quantitative 67. Shaw RG, Byers DL. 1998. Genetics of genetics. Chapman and Hall, NY, USA. maternal and paternal effects. pp. 97-111 in 57. Roitberg BD. 1998. Oviposition decisions Mousseau TA, Fox CW (eds.) Maternal as maternal effects: Conundrums and Effects as Adaptations. Oxford University opportunities for conservation biologists. Press, New York, USA. pp. 67-79 in Mousseau TA, Fox CW (eds.) 68. Siemens DH, Johnson CD. 1990. Host- Maternal Effects as Adaptations. Oxford associated differences in fitness within and University Press, New York, USA. between populations of a seed beetle 58. Rossiter M. 1991. Environmentally-based (Bruchidae): effects of plant variability. maternal effects: a hidden force in insect Oecologia 82: 408-423. population dynamics. Oecologia 87: 288- 69. Siemens DH, Johnson CD. 1992. Density- 294. dependent egg parasitism as a determinant 59. Rossiter M. 1993. Initiation of maternal of clutch size in bruchid beetles effects in Lymantria dispar: Genetic and (Coleoptera: Bruchidae). Environmental ecological components of egg provisioning. Entomology 21: 610-619. Journal of Evolutionary Biology 6: 577-589. 70. Siemens DH, Johnson CD, Ribardo KV. 60. Rossiter M. 1994. Maternal effects 1992. Alternative seed defense mechanisms hypothesis of herbivore outbreaks. in congeneric plants. Ecology 73: 2152- Bioscience 44: 752-762. 2166. 61. Rossiter M. 1996. Incidence and 71. Siemens DH, Johnson CD, Woodman RL. consequences of inherited environmental 1991. Determinants of host range in bruchid effects. Annual review of Ecology and beetles. Ecology 72: 1560-1566. Systematics 27: 451-476. 72. Siemens DH, Ralston BE, Johnson CD. 62. Rossiter M. 1998. The role of environmental 1994. Alternative seed defense mechanisms variation in parental effects expression. pp. in a paloverde (Fabaceae) hybrid zone: effects on bruchid beetle abundance. 1427. Ecological Entomology 19: 381-390. 77. Via S. 1994. The evolution of phenotypic 73. Smith CC, Fretwell SD. 1974. The optimal plasticity: what do we really know? pp. 35- balance between size and number of 57 in Real LA (ed.) Ecological genetics. offspring. The American Naturalist 108: Princeton University Press, Princeton, NJ, 499-506. USA. 74. Thornhill R, Alcock J. 1983. The evolution 78. Wade MJ. 1998. The evolutionary genetics of insect mating systems. Harvard of maternal effects. pp. 5-21 in Mousseau University Press, Cambridge, MA USA TA, Fox CW (eds.) Maternal Effects as 75. Vahed K. 1998. The function of nuptial Adaptations. Oxford University Press, New feeding in insects: a review of empirical York, USA. studies. Biological Reviews 73:43-78. 79. Wrensch DL, Ebert MA (eds.). 1993. 76. Via S. 1991. Specialized host plant Evolution and diversity of sex ratio in performance of pea aphid clones is not insects and mites. Chapman and Hall, Inc., altered by experience. Ecology 72: 1420- New York, NY, USA.