Maternal Effects in Insect-Plant Interactions:

Maternal effects occur when the phenotype or environment of a mother affects the phenotype of her offspring via some mechanism other than the transmission of genes. The primary objective of this review is to use examples from my own research on the interaction between seed beetles and their host plants to illustrate how maternal effects influence ecological interactions in nature. I explain how maternal effects generate many patterns observed in nature. I also discuss how maternal effects may be influenced by the genotypes of females or their progeny and can thus respond to natural selection and evolve. I will emphasize that maternal effects often evolve as mechanisms by which females can manipulate the phenotype of their progeny to prepare them for environmental conditions that they will encounter (adaptive crossgenerational phenotypic plasticity). Introduction Early in the 20 century animal and plant breeders developed a simple conceptual framework within which they could quantify sources of phenotypic variation within populations and understand the consequences of this variation for the production of new strains of agricultural plants and animals. In this framework, phenotypic variation among individuals (VP) is partitioned into a component due to genetic differences among individuals (VG), another due to environmental differences among individuals (VE), and the interaction between these components, producing the now standard quantitative genetic relationship VP = VG + VE + interactions (10, 56). Each of these components (VG, VE, and interactions) can be further subdivided into sub-components (such as dominance variation, additive genetic variation, etc.). This simple framework has proven invaluable for understanding responses of agricultural plants and animals to artificial selection − the response to selection is easily predicted if you know the magnitude of natural selection and the proportion of phenotypic variation in a population that is due to genetic differences among individuals. Ecologists working with natural systems also use this simple framework for understanding selection in natural systems, and a large body of literature has blossomed in which techniques of quantitative genetics are applied to nonagricultural organisms (review in 56). This conceptual framework is invaluable for understanding evolutionary processes in nature because it has focused our attention on analyses of genetic differences among individuals (the VG in the above equation). Such differences are basis for responses to natural selection. In this manuscript I will attempt to convince readers that some types of environmental variation (the VE in the above equation) can also be of ecological and evolutionary importance. Specifically, I will discuss mechanisms by which phenotypes of mothers or the environments they experience can affect the phenotypes of their progeny. Until very recently researchers have rarely considered or measured the impact of environmental effects experienced in previous generations on contemporary phenotypic expression (55, 50, 51, 52). I will argue here that maternal effects produce many of the patterns that we observe in nature and that the study of maternal effects is very important for understanding the evolution of many types of ecological interactions. Using examples from my own work, I will explain how maternal effects generate many patterns observed in nature and how they influence population responses to natural selection. I also will discuss how maternal effects may be influenced by the genotypes of females or their progeny and can thus respond to natural selection and evolve. I will emphasize that maternal effects often evolve as mechanisms by which females can manipulate the phenotype of their progeny to prepare them for environmental conditions that they will encounter (adaptive crossgenerational phenotypic plasticity). What are Maternal Effects? In the simplest terms, maternal effects occur when the phenotype or environment of a mother affects the phenotype of her offspring via some mechanism other than the transmission of genes (50, 51, 52). By this definition, I exclude the inheritance of genes in cytoplasmic organelles (mitochondria and chloroplasts) from being considered a maternal effect; they are inherited through mothers but are better classified as traits that are inherited via non-Mendelian genetic inheritance rather than as a maternal effect. Maternal effects are a fundamental consequence of the differences in reproductive biology between males and females – mothers provide much of the environmental context within which progeny develop and progeny genotypes are expressed (78) while in most organisms males provide little more than small gametes. Mothers determine how many resources are allocated to eggs (13, 14, 17), what type of resources are allocated to eggs (1), and when and where eggs are laid (57). In some taxa mothers even determine the sex of their progeny (79). After egg production, mothers generally determine how much parental care their progeny receive, although fathers provide parental care in a few insects (e.g., 74). All of these maternal “decisions” are chances for a mother’s phenotype or environment to influence the phenotype of her progeny (e.g., 25). Maternal effects have been identified across a wide variety of taxa and for a wide variety of traits (50, 51, 52, 61, 62). One of the most commonly observed maternal effects is the influence of maternal age on the phenotype of her progeny (54). In vertebrates and many aquatic and marine arthropods females tend to produce larger progeny as they get older (e.g., 2), but females of most insect species produce smaller progeny as they get older (17). The seed beetle Callosobruchus maculatus (Coleoptera Bruchidae) exhibits the typical insect pattern – older females produce smaller eggs than younger females (Fig. 1a) and progeny hatching from these smaller eggs tend to have lower survivorship and take longer to reach maturity (Fig. 1b), although they tend to mature at roughly the same size as their siblings that hatched from eggs laid by their mother when she was younger (11, 20). Thus, a maternal effect explains much of the phenotypic variation in survivorship and development time within a single family; progeny from older females hatch from smaller eggs and must compensate for their small size by extending development time to eventually mature at a normal body size. Maternal effects can also explain much of the phenotypic variation among families. For example, although the size of egg that a female lays decreases with increasing age, the rate of this decrease varies among females depending on their nutritional status (Fig. 1a). Females that have ready access to food and water or access to extra mates (from which they obtain nutritional contributions) exhibit a slower decline in egg size as they get older (11). This influence of maternal nutritional status on egg size translates into effects on progeny growth − progeny hatching from eggs produced by well fed females mature sooner than progeny hatching from eggs laid by food-stressed females (Fig. 1b; 11, 20). Oviposition decisions made by a female, such as where to lay her eggs or how many eggs to lay in a locality, will influence the environment within which her offspring will develop (47, 57). In most seed beetles (Coleoptera: Bruchidae) larvae develop inside a single host seed and are incapable of moving among seeds. Females of many species will either lay clutches (23) or will readily superparasitize seeds (22; but see 47, 48). Each additional egg that a female lays on a seed reduces the amount of resources available for the larvae (including her progeny) inside the seed. Fortunately for the larvae, many species have evolved developmental plasticity in which larvae can mature at a smaller than normal body size when reared under intense larval competition (Fig. 2a; but see 46). Thus, when females lay multiple eggs per seed their progeny mature at a smaller size than progeny reared at lower densities (e.g., 15, 19, 27). These smaller progeny produce smaller eggs (and have lower fecundity), which influences the phenotype of the next generation. In C. maculatus, progeny hatching from these smaller eggs eventually mature at a smaller size (Fig. 2b; 13, 14). In both Stator limbatus and S. pruininus progeny hatching from these smaller eggs extend development time to eventually mature at a normal body size (the size at which 0 0.5 1 2.5 3 4.5 5 5.5 6 6.5 7 7.5 8 Maternal Age (days) 0.30 0.32 0.34 0.36 0.38 0.40 Eg g W id th (m m ) Fed females Starved females 0 0.5 1 2.5 3 4.5 5 5.5 6 6.5 7 7.5 8 Maternal Age (days) 30 32 34 36 38 D ev el op m en t T im e (d ay s) Figure 1 (a) Female Callosobruchus maculatus produce progressively smaller eggs as they get older. (b) This decline in egg influences the egg-to-adult development time of a female's progeny (development time of female progeny is shown). Note that the rate at which egg size decreases with age depends on the female's nutritional status − egg size decreases more slowly for females that have access to food (shown) or that obtain multiple ejaculates from males, and this influence on egg size corresponds to a change in progeny development time. Data from 11 and 20. they would have matured if reared at low density; Fig. 2c; 15, 19). In each case we can demonstrate that these differences in body size (C. maculatus) or development time (both species of Stator) are environmental effects inherited through mothers by crossing progeny from lines reared at high density with lines reared at low density. In these crosses we observe that the size of C. maculatus progeny (at maturation; Fig. 2b) and the development time of Stator progeny (Fig. 2c) are each influenced entirely by the density at which their mother was reared. Paternal density has no effect of the phenotype of progeny in either species (Fig. 2b and 2c). These experiments demonstrate two points. First, maternal oviposition decisions can affect the phenotypes of both their progeny and their grand-progeny; females that lay multiple eggs per seed produce smaller progeny, that in turn produce smaller eggs, which in turn affects the development time or body size of the grandprogeny. This is a maternal effect. Second, even though both Callosobruchus and Stator have very similar life cycles, the two beetles exhibit very different types of maternal effects in response to similar ecological stresses (in this case, high larval density). Thus, the form in which maternal effects are exhibited can vary substantially among organisms (e.g., influences on development time vs. body size), even when those organisms are ecologically quite similar. Paternal Effects Although I will focus on maternal effects in this manuscript, I want to acknowledge that paternal effects (the influence of a father's genotype or environment on the phenotype of his progeny) are probably more common in nature than previously suspected. In most insects, males contribute large ejaculates, spermatophores or other accessory gland 1 3 5 7 9 11 13 15 17 19 21 Larval Density (beetles per seed) 3.5 4.0 4.5 5.0 5.5 Fe m al e M as s ( m g) L L L H H L H H Cross 5.1 5.2 5.3 5.4 5.5 B od y M as s ( m g) L L L H H L H H Cross 23.0 23.5 24.0 24.5 25.0 D ev el op m en t T im e (d ay s) Callosobruchus