Maternal effects and the population dynamics of insects on plants

If, like me, your mother continues to interfere in your life, far beyond her genetic contribution to your phenotype, then you may be sympathetic to the concept of maternal effects and their influence upon organismal ecology. Non-Mendelian maternal effects describe the transfer of information from the maternal environment to the phenotype of offspring (Mousseau & Fox, 1998). In essence, many aspects of the parental environment (climate, food quality, natural enemies) can influence the allocation of resources by parents to offspring and the quality of parental care. Before you scream ‘Lamarck’ and run for your copy of The Selfish Gene (Dawkins 1976), non-Mendelian maternal effects do not result in heritable (genetic) change in offspring. Rather, they describe the contribution of the parental environment to phenotypic variation in progeny. What does this have to do with the population ecology of agricultural and forest pests? My interest in maternal effects was reawakened recently at the combined meeting of the Royal Entomological Society and the International Union of Forestry Research Organizations in Aberdeen, Scotland (September 2001). At the meeting, I heard two presentations in which the expression of maternal effects could be inferred to explain patterns of population change in pest insects. In the first presentation, Werner Baltensweiler described the analysis of 50 years of data on the larch budmoth, Zieraphera diniana (Baltensweiler & Rubli, 1999). The larch budmoth has been considered to provide a classic case of population cycles driven by insect-mediated changes in plant quality (Baltensweiler, 1984; Baltensweiler & Fischlin, 1988). Declines in needle size and nitrogen concentration during budmoth outbreaks have been thought to provide the time-lagged negative feedback necessary to drive population cycles. However, at the conference, Baltensweiler reported that it may not be that simple. Towards the end of his 50-year dataset, reductions in needle size were not apparent during outbreaks, yet cycles continued as before. Having previously discounted the influence of natural enemies on population cycles, Baltensweiler suggested that time-lagged maternal effects may be responsible for cyclic dynamics. In a second presentation, Vince Nealis reported that the overwintering survival of spruce budworm (Choristoneura fumiferana) larvae was a major factor in population declines of budworm at the end of outbreaks. Budworm larvae hatch in the autumn and generally do not feed before entering winter diapause (Royama, 1992). Consequently, their resources for surviving the winter are provided entirely by the maternal provisioning of eggs. Nealis noted that declines in winter survival were associated with changes in the species composition of forest stands from which one might conclude (at least, I did) that changes in maternal diet may be responsible for changes in egg provisioning and subsequent declines in larval survival. The tremendous effort that has gone in to the collection of long-term data on spruce budworm and larch budmoth has yielded tantalizing glimpses of the possible action of maternal effects in pest population dynamics. Because few of us have collected population datasets even approaching the length of these classics, we have to hope that there exist faster ways to assess the prevalence of maternal effects in our own systems of study. Here, I explore what we know to date about the action of maternal effects and their potential to influence pest population dynamics. Maternal effects are ubiquitous in natural and managed ecological systems (Bernardo, 1996; Mousseau & Fox, 1998a). Organisms as diverse as baboons (Alberts, 1994), barnacles (Holm et al., 2000) and salamanders (Collazo, 1993) all exhibit maternal effects on offspring performance. The term ‘maternal effect’ is generally used as a shorthand for non-Mendelian parental effects, which can include contributions from the father as well as from the mother. For example, environmentally determined variation in the quality of male ejaculate as a resource for females would be considered as a paternal effect (Savalli & Fox, 1998) if it influenced the phenotype of offspring. For simplicity, I will stick with current convention and use the phrase ‘maternal effect’ to describe all non-Mendelian parental effects of both maternal and paternal origin. The forms and consequences of maternal effects are remarkably varied. A few of my favourites from the recent literature include maternal effects upon the size of cultured edible snails (Dupont-Nivet et al., 1997) and the glancing rate of infant baboons (Alberts, 1994). I was also amused to discover that both hormones and vaginocervical stimulation are required for the induction of maternal behaviour in sheep (Kendrick & Keverne, 1991). Of course, not every trait expressed by offspring is influenced by maternal effects. I am happy to report that male licking behaviour does not appear to have a maternal component, at least in Drosophila (Welbergen & Van Dijken, 1992). However, many of the traits that we do know to be important for population dynamics (Rossiter, 1991a, 1992, 1994; Ginzburg & Taneyhill, 1994; Benton et al., 2001) and rates of evolutionary change (Bernardo, 1996; Rossiter, 1996, 1997; Mousseau & Fox, 1998a; Wolf et al., 1999; Brodie & Agrawal, 2001) have strong maternal effects components. These include offspring survival, dispersal, growth rate, diapause and fecundity. There is also growing evidence that some maternal effects are not simply the accidental transmission of environmental information from one generation to the next. Rather, in many cases, the form and function of maternal effects appear to have been shaped by natural selection (Mousseau & Fox, 1998b). In many organisms, a female's environment provides a reliable indicator of the environmental conditions that her progeny will encounter. In such cases, maternal effects may evolve as mechanisms for transgenerational phenotypic plasticity, whereby, in response to a predictive environmental cue, a mother can change the type of eggs that she makes or can programme a developmental switch in her offspring, which produces offspring prepared for the environmental conditions predicted by the cue (Fox et al., 1999a). The first to recognize the potential for maternal effects to influence population dynamics were Wellington (1957) and Leslie (1959). Both pointed out that the phenotypic traits expressed by individuals within populations could vary among generations, leading to variation in susceptibility to environmental challenges. For example, Wellington (1957) tracked variation in the behaviour and performance of western tent caterpillars, Malacosoma pluviale, through different stages of population growth and concluded that dynamics were influenced by the changing quality of individuals. He developed this theme in subsequent work (Wellington, 1960, 1964) and came to the conclusion that population biologists ‘sometimes act as though they … have forgotten the animals from which their disciplines sprang’ (Wellington, 1977). In other words, populations are not lumps of phenotypically identical protoplasm that remain invariant within and among years. Maternal effects provide a mechanism by which the environment in a given year is expressed in the phenotypic variation of offspring in subsequent years (Rossiter, 1994) and therefore provide a route of delayed negative feedback (Berryman, 1999). It is well established that delayed density dependence can destabilize population dynamics and promote cyclic dynamics (Schaffer & Kot, 1986; Turchin, 1990; Royama, 1992). Exactly how is environmental information transferred between parental and offspring generations? One mechanism by which females influence the phenotype of their progeny is through heterogeneity in egg quality, in which females vary egg size and egg provisioning (Rossiter, 1991a,b; McIntyre & Gooding, 2000). Mothers who provide significant resources to their offspring by provisioning their eggs are essentially transmitting components of their own environment to that of their offspring in an oocytic ‘packed lunch’, and differential allocation by mothers of resources to eggs has become a classic example of a maternal effect (Rossiter, 1991a,b; Gliwicz & Guisande, 1992; Rossiter et al., 1993; Rolff, 1999). In some cases, the transmission of maternal environment to the offspring may simply reflect the non-adaptive legacy of previous conditions. Overall reductions in egg provisioning or larval performance when mothers are reared in poor environments provide examples of this type of maternal effect in insects (Gould, 1988; Jann & Ward, 1999; McIntyre & Gooding, 2000). The tragedy of ‘crack babies’ provides an example from humans. Nevertheless, maternal effects are not always the passive transmission of good or bad parental experiences to offspring. Egg provisioning in many species is a plastic trait in which environmental conditions influence the expression of the trade-off between egg size and egg number. In such cases, adaptive changes in resource allocation to offspring under varying environmental conditions can be considered as a form of flexibility in ‘family planning’. For example, Daphnia mothers grown under conditions of low food availability produce a few large offspring that are able to withstand some degree of starvation. In contrast, mothers grown under conditions of high food availability produce many more offspring that are not resistant to starvation (Gliwicz & Guisande, 1992), presumably because their offspring are unlikely to encounter significant food deprivation. In a similar kind of study, Kim & Thorp (2001) report that the solitary bee, Megachile apicalis, varies seasonally the allocation of resources to eggs. Spring females produce many small offspring, whereas summer females produce a few larger offspring. The production of large offspring later in the season is considered to increase the probability of overwintering survival. Recent work suggests that maternal effects acting upon the egg size/egg number trade-off may be adaptive primarily for the mother, increasing her fitness at the expense of offspring fitness (Einum & Fleming, 2000). Of course, parental care can extend well beyond the provisioning of eggs, and much of that care can be envisaged as a sort of protracted ‘packed lunch’. At its most simple, post-hatch care can include the provisioning of resources for larvae in the absence of contact with the parent (dinner is in the fridge, so to speak). However, the resources provided need not always be nutritional. For example, when females of the desert tenebrionid, Parastizopus armaticeps, are provided with supplementary food, they do not increase allocation to their young. Rather, they spend less time foraging and more time aiding males in digging natal burrows. The depth of natal burrows is related to larval survival because deep burrows reduce the probability of desiccation (Rasa, 1998). In this case, moisture rather than food represents the currency of the maternal effect, even though the availability of food for the mother initiates the effect. The longer-term consequences of parental provisioning can be dramatic. For example, larvae of the long-horned dung beetle Onthophagus taurus are provided with fragments of dung before the departure of their parents. In a fascinating example of a paternal effect, males that aid females in the provisioning process produce sons with horns, whereas males that do not help provision the nest produce males without horns. The extra dung provided by the helpful males is sufficient to induce horn production in their male offspring (Hunt & Simmons, 2000). The effects of such paternally determined variation in morphology for the population ecology of the beetles is unclear, but is very likely to influence the competitive ability of male beetles. In other words, maternal effects can influence the phenotype of offspring well beyond the first few days or weeks of life. In the outbreak insect, Epirrita autumnata, maternal environment still influences the consumption and growth of fifth-instar larvae and their subsequent pupal mass (Alonso et al., 2001). Given that pupal mass is a reliable indicator of fecundity in E. autumnata, maternal effects have a clear potential to influence population growth. The pupal mass of Papilio butterflies is also influenced by maternal diet (Thompson et al., 1990). Maternal effects can be of even longer duration. For example, egg-to-adult viability in Drosophila serrata is dependent upon both maternal and grandmaternal effects (Hercus & Hoffmann, 2000). Similarly, the ‘telescoping generations’ of many aphids, whereby the development of grandchildren commences within the grandmaternal body (Mousseau & Dingle, 1991), provides a substantial time-lag between the current environment and the expression of phenotype in offspring. Lest we consider grandparental effects as unique to insects, studies have shown that the mass of deer fawns and their susceptibility to wolf predators is a function of both maternal and grandmaternal environment (Mech et al., 1991). The life-history traits that are influenced by maternal effects are many and diverse (Mousseau & Dingle, 1991). For example, maternal effects have been invoked to explain variation in fly mating behaviour (Mangan, 1991), adult morphology (Bryant & Meffert, 1998), the choice of pupation site (Bauer & Sokolowski, 1988) and the competitive ability of offspring (McIntyre & Gooding, 2000). Maternal effects are the most important determinant of head width in alfalfa leafcutting bees, Megachile rotundata (Owen & McCorquodale, 1994) and a significant contributor to variation in the body size of adult carabid beetles (Desender, 1989). Maternal effects may be mediated by the interaction of mothers with natural enemies in the environment. For example, in the damselfly Coenagrion puella, a high ectoparasite load (Acari: Arrenurus cuspidator) on mothers stimulates the production of fewer, larger offspring (Rolff, 1999). Although the adaptive value, if any, of this maternal response is unclear, changes in offspring size and number have the potential to influence damselfly population dynamics. Within a single of eggs, some insects may resources upon the of more resources to eggs with low of than they do to eggs with a of et al., In this case, their eggs from predators and are more likely to eggs from the of than from the et al., 1997; 2001). eggs are larger than at the of the Of course, maternal effects can also act to the response of individuals to in the environment. For example, production by the to an increase in because the of eggs within the body to be determined by environmental 1999). time-lag in response to environmental conditions is the kind of effect that can influence subsequent population The natural enemies of insects are to maternal effects, and such effects have the potential to influence the population dynamics of both enemies and their For example, the of the declines in in because the fecundity of the is determined by maternal effects et al., 1992). Similarly, both development time and body mass of the and are influenced by maternal effects & 1994; et al., a of population can be influenced by maternal effects, and two appear to be the environment by the mother can influence the of her offspring to 1993; & 1997; & et al., maternal environment can the probability that the offspring will the process & of the in the production by is a classic case in which the environment of the mother (climate, density and food influences the phenotype and ability of her offspring I that many would that the production of and a generation has influence on population and this may be the between maternal effects and population change of which we are in ability have also been noted in other For example, the of larvae to from their egg is related to the environmental of the mother et al., the of and offspring by some is influenced by maternal effects & maternal effects are a of change in and to the production of the forms that are so to et al., 1994). The influence of maternal environment on survival during is much to as a examples However, variation in during of the is entirely dependent upon the foraging and subsequent mass of the mother & The of beetles has provided the expression of maternal effects. Maternal effects may influence adult and (Fox et al., & 1997; & egg size and viability 1993; et al., larval survival (Fox et al., & 2000) and the development time of larvae 1993; et al., ejaculate size of male a significant contributor to may be influenced by maternal effects (Savalli & Fox, 1998). for population the expression of maternal effects in beetles can be density dependent (Fox & the for in the action of and the potential induction of population cycles (Rossiter, 1991a, 1994). you are a are that your environment has a major on your life. and studies of and have provided a of information on the expression of maternal effects. variation by mothers can influence size & the morphology of & and components of the of males & 1992). most for population maternal effects can have a strong influence on the induction of diapause and subsequent (Mousseau & et al., 1990; 1994). For insects in rates of population growth can be by the number of year et al., & diapause is the environment by mothers can promote continued development when conditions are or induce diapause when conditions are & 2000). maternal effects have been shown to influence diapause in & & 1991), & et al., & & 1998) and & when is for a given species of insect, maternal effects are of the (Mousseau & Dingle, 1991). 1960, 1964) the expression of maternal effects in has less than it However, there are examples maternal effects have been shown to influence a of phenotypic traits related to population dynamics (Gould, 1988; Rossiter, 1992, 1994; Rossiter et al., 1993; et al., 1996; & 1998). For example, the of the parental diet can influence the performance of with the expression of the maternal effect dependent upon offspring environment (Gould, 1988). the also maternal effects. in parental required for development of larval offspring, can have or negative effects upon the larvae of upon the are from or species & 1998). Similarly, in the parental diet of the the fitness of offspring of the diet that they and for of the phenotypic in larval performance et al., 1998). environmentally maternal effects have been shown to influence the phenotypic traits of larvae and and provide an example of the development of a of population dynamics from studies of and maternal effects. In studies of the and ecology of use by the (Rossiter, Rossiter et al., Rossiter that the susceptibility of larvae to the was determined in by maternal provisioning of eggs et al., 1990). In subsequent studies of egg Rossiter reported that from large eggs faster and pupal and than from small eggs (Rossiter, Although egg size a genetic component, there was also a strong influence of maternal diet and maternal effects to offspring development and fecundity. For example, mothers reared on of offspring with than mothers reared on (Rossiter, In the concentration of the maternal diet was related both to the length of the larval and to the pupal mass of parents were on two different parental diet for of the in larval development whereas offspring diet for These Rossiter to that maternal effects could a in the population dynamics of the work by Rossiter developed two studies of the and consequences of maternal provisioning et al., 1996; & Rossiter, and the development of of population dynamics that time-lagged contributions of maternal effects (Rossiter, 1996, 1998). For example, the in eggs is In and as parental maternal diet was to influence in eggs et al., In the of the egg was related to in the eggs from the parental diet et al., In her Rossiter the consequences of time in the expression of environmental conditions for population from and outbreak dynamics (Rossiter, 1994). Maternal effects have the potential to the density and quality of individuals from other in the quality and the density of natural with many time-lagged maternal effects can population and cyclic dynamics (Berryman, 1999). work has both & & 1996; & 1999; Benton et al., 2001) and et al., & et al., 2001) studies of the of maternal effects in population dynamics. The work has the for maternal effects population and the between and the that they & 1994; Benton et al., 2001). when about the in which to maternal effects, all that they have the potential to population cycles and may be to from other of delayed negative feedback (Berryman, 1999; Benton et al., 2001). has been less in studies of maternal effects in natural studies of the have reported effects of maternal environment on offspring performance et al., 1996; & Rossiter, whereas two other studies have not et al., & 2000). However, in my all studies are In case, eggs or larvae were collected from different populations that in their population population population population on larval dispersal, survival growth were then to the that individuals from similar on the population would phenotypic traits in because of maternal studies are therefore examples of in which populations at different growth stages are used to changes in a single population The is that maternal effects, by their very are not to The studies do a of or not populations at a of growth phenotypic do not a of the that changes in maternal provisioning within a single site time are associated with population dynamics. The is females change their allocation to eggs time as environmental conditions not allocation patterns are in similar to of other In other words, there may not be a of phenotype among populations at the of growth. However, population may exhibit variation in allocation time and time-lagged effects on performance sufficient to population cycles. has been in the the expression of maternal effects varies in and there is to between maternal effects and population dynamics in natural populations time (Wellington, 1988; 1991). studies of quality, and the environment and are required for an of the maternal effects of outbreak (Rossiter, 1994). The current of is that there strong evidence from studies to that maternal effects influence the life-history traits of that maternal effects provide the potential for delayed negative feedback in and a delayed negative feedback to population outbreaks and cycles. What we are still is clear evidence of population dynamics in the that are driven by maternal effects. Although the work reported by Baltensweiler and by Nealis in is of maternal effects, of and effect has pointed it will be to the influence of maternal effects from other delayed negative feedback such as declines in plant quality or the influence of natural Maternal effects therefore among the of other ecological that be with a of data and analysis et al., 1997; & & 2001). of maternal effects in population dynamics have the that are and studies be within single maternal effects will to be major of population change is not yet However, it is clear that or to maternal effects may result in of and or not such effects are a of the (Mousseau & Dingle, I would like to the for our work on the population dynamics of I would also like to my mother for her continued genetic and in my life.