Maternal Effects in Insect-Plant Interactions: Lessons from a Desert Seed Beetle
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Maternal Effects in Insect-Plant Interactions: Lessons From a Desert Seed Beetle 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 animals. 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 beetles 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 animal 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 insects (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 arthropods 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 Stator 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.