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Anaphes Nitens DOI: 10.1111/j.1570-7458.2007.00595.x Blackwell Publishing Ltd Maternal size and age affect offspring sex ratio in the solitary egg parasitoid Anaphes nitens Serena Santolamazza-Carbone1*, Montserrat Pestaña Nieto1 & Adolfo Cordero Rivera2 1Centro de Investigación e Información Ambiental de Lourizán, Sección de Fitopatología, Apartado de Correos 127, Lourizán, Pontevedra, Spain, 2Grupo de Ecoloxía Evolutiva e da Conservación, Departamento de Ecoloxía e Bioloxía Animal, Universidade de Vigo, EUET Forestal, Campus Universitario, Pontevedra, Spain Accepted: 3 May 2007 Key words: biological control, nutritional status, fecundity, clutch size, Gonipterus scutellatus, Hymenoptera, Mymaridae, Eucalyptus Abstract In this study, the effects of maternal age, diet, and size on offspring sex ratio were investigated for the solitary egg parasitoid, Anaphes nitens Girault (Hymenoptera: Mymaridae), both outdoors, during the winter, and inside a climatic chamber under favourable constant conditions. During the winter of 2005–2006, each of seven groups containing 40 1-day-old females was mated and randomly distributed among two treatments: (treatment 1) a droplet of undiluted honey ad libitum + one fresh egg capsule of the snout beetle Gonipterus scutellatus Gyllenhal (Coleoptera: Curculionidae) as host; (treatment 2) drops of water + one fresh egg capsule of G. scutellatus. We recorded the lifetime fecun- dity, the daily sex allocation, and the lifetime offspring sex ratio to study the existence of a relationship with maternal characteristics. Moreover, we assessed the effect of location (outdoors vs. indoors) and group (groups are representative of early, mid, and late winter) on sex ratio. The most important factor that biased the sex ratio was maternal body size: larger females of both treatments produced more female offspring. As females of A. nitens could gain more advantage than males from body size, larger mothers have a higher fitness return if they produce more daughters. The effect of the treatment was significant: starved females produced more females. Location and group were not significant. Fecundity and sex ratio were age dependent. Old mothers that received honey (treatment 1) had fewer offspring and a more male-biased offspring sex ratio, probably due to reproductive senescence and sperm depletion. Starved females (treatment 2) experienced reproductive decline earlier, perhaps because they invested more energy in maintenance rather than in reproduction. daughters she has produced, then the benefit of producing Introduction males and females is not equal, but depends on offspring In parasitic Hymenoptera, mated females store sperm in mating opportunities (Godfray, 1994). Female-biased sex the spermatheca and can manipulate the sex ratio (males/ ratios are common among hymenopterous parasitoids total offspring) of their progeny by controlling fertilization that live in subdivided populations, with a few foundresses during oviposition. The haplodiploid sex-determination inside the patch and some degree of sib-mating (Hamilton, system (arrhenotokous parthenogenesis) provides the 1967; Antolin, 1993; Hardy, 1994). mothers with a mechanism to control progeny sex ratio, In the context of the study of sex allocation, attention because males develop from unfertilized eggs (haploid) and has been focused especially on resources (host and food) females from fertilized eggs (diploid) (Gould & Bolton, quality and abundance, to which the females are expected 1996). If we measure maternal fitness by adding the to respond in an adaptive way. The consequences of host number of mates of her sons to the lifetime number of abundance (Bai & Smith, 1993; King et al., 1995), host size (Charnov et al., 1981; King & Lee, 1994; Heinz, 1996; Napoleon & King, 1999), host age (King, 2000), host *Correspondence: Serena Santolamazza-Carbone, Centro de Investigación e Información Ambiental de Lourizán, Sección de species (King, 1987; Uçkan & Gülel, 2002), and host quality Fitopatología, Apartado de Correos 127, Lourizán, 36080 Pontevedra, (healthy vs. parasitized) (King, 1996a; van Baaren et al., Spain. E-mail: [email protected] 1999) on sex ratio have been intensively studied during © 2007 The Authors Entomologia Experimentalis et Applicata 125: 23–32, 2007 Journal compilation © 2007 The Netherlands Entomological Society 23 24 Santolamazza-Carbone et al. the last two decades, generating important theories and Moreover, if the reproductive success varies seasonally, guidelines for practical applications in biological control mothers may use variation in abiotic factors as seasonal programmes. Evolutionary models, such as the local mate cues to predict future mating opportunities for their off- competition model (Hamilton, 1967; Werren, 1983; Cook spring (Godfray, 1994). et al., 1994; Hardy, 1994), which study the consequences of Anaphes nitens Girault (Hymenoptera: Mymaridae) is a female wasp density inside the patch, and other models solitary, idiobiont egg parasitoid of the Eucalyptus snout related to the response to adult sex ratio inside the popula- beetle Gonipterus scutellatus Gyllenhal (Coleoptera, Cur- tion, such as the perturbation model (Werren & Charnov, culionidae) (Tooke, 1955). This wasp was introduced to 1978), the constrained females model (Godfray, 1990), or northwestern Spain in 1992 as a biocontrol agent of the the crowding model (Waage, 1982), explain the existence weevil, quickly obtaining excellent results (Cordero Rivera of adaptive mechanisms that mothers adopt to increase et al., 1999). Gonipterus scutellatus females lay clumped their fitness through sex ratio manipulation (King, 1996b). eggs on young Eucalyptus spp. leaves and cover the eggs with On the other hand, maternal characteristics, such as age, a dark secretion mainly composed of faeces, which becomes egg load, diet, size, experience, time until mating, or number hard after some hours (so-called egg capsule). The egg of matings (King, 1987), are also important factors that capsules contain a mean of 8–10 eggs (Tooke, 1955). This shape sex allocation; however, in comparison with host situation makes A. nitens a parasitoid whose offspring variables, these have received less attention. The relation- develops in a quasigregarious fashion, because even if the ship between maternal age and offspring sex ratio could be larvae develop alone, the adults emerge together. Females more complicated than expected, because, depending on are weakly synovigenic, because they are born with a the ovigeny index and mating opportunities, old females mean egg load of 46 eggs, which can be increased by may experience an increase, a decrease, or no change of the about 20% during adulthood (Santolamazza Carbone & offspring sex ratio (King, 1987). In general, reduction of Cordero Rivera, 2002); under natural conditions, egg the female ratio among offspring when the mother is aged resorption can take place especially among starved is due to sperm depletion or reduced sperm viability, females (S Santolamazza-Carbone, M Pestaña Nieto & A but if the mother chooses to mate again, sex ratio may Cordero Rivera, unpubl.). Previous investigations have decrease. shown that this parasitoid adopts a female-biased sex ratio Maternal size could affect offspring sex ratio, as in the both in the field (male proportion = 0.24 ± 0.01) and in aphid parasitoid Aphytis melinus, where the positive rela- the laboratory (0.28 ± 0.04), that superparasitism usually tionship between maternal age and sex ratio is true only for increases male progeny (0.40 ± 0.07), and that the classical large females because they live longer and exhaust their local mate competition theory does not completely explain sperm supply (King, 1987). Large size may also improve the sex ratio estimated in the field under different conditions the female’s ability to obtain larger hosts, which are generally of population density (Santolamazza Carbone & Cordero used to produce daughters (Seidl & King, 1993; Heinz, 1996). Rivera, 2003). On the other hand, paternal characteristics such as age, Until now, no data are available on the effect of maternal time elapsed between matings, or the number of matings characteristics on offspring sex ratio in A. nitens. Hence, could also influence quality and size of ejaculates, produc- the main aim of this work was to test the effect of biotic ing biased sex ratios (King, 1987). Sperm replenishment factors such as maternal age, size, and nutritional status on requires a variable amount of time, thus the male ability to offspring sex ratio. Moreover, by conducting the experi- fertilize after a first mating could be weak if males mate in ments outdoors and inside a climatic chamber, we tested rapid succession (Damiens & Boivin, 2005). the effect of temperature (constant indoors and naturally As female access to food could enhance longevity, it fluctuating outdoors) on sex-ratio bias. If sperm supply should also contribute to variation in sex-ratio decisions. constitutes a limiting factor for our study species, then we In Bracon hebetor, for example, well-fed mothers live longer expected that old females should produce more sons. and produce more females (Rotary & Gerling, 1973). Also, Furthermore, if body mass is maternally inherited and environmental factors such as photoperiod, temperature, large females tend to produce larger offspring, as in and humidity may bias offspring sex ratio because they A. nitens (S Santolamazza-Carbone, M Pestaña Nieto, R may cause differential mortality of male and female pro- Pérez
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