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Reproduction and Offspring Sex Ratios Differ Markedly Among Closely Related Hyperparasitoids Living in the Same Microhabitats

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Reproduction and Offspring Sex Ratios Differ Markedly Among Closely Related Hyperparasitoids Living in the Same Microhabitats J Insect Behav (2019) 32:243–251 https://doi.org/10.1007/s10905-019-09730-z Reproduction and Offspring Sex Ratios Differ Markedly among Closely Related Hyperparasitoids Living in the Same Microhabitats Jeffrey A. Harvey & Lucas de Haan & Oriol Verdeny-Vilalta & Bertanne Visser & Rieta Gols Received: 2 May 2019 /Revised: 2 October 2019 /Accepted: 12 October 2019 /Published online: 25 October 2019 # The Author(s) 2019 Abstract Closely related species in nature usually ex- times higher in G. proximus than in G. agilis with hibit very similar phylogenetically conserved traits, such G. hortensis producing intermediate numbers of off- as reproduction, behavior and development. Here, we spring. All three species depleted their teneral reserves compared fecundity schedules, lifetime reproductive during their lives. Females of G. proximus and success and offspring sex ratios in three congeneric G. hortensis lived significantly longer than females of facultative hyperparasitoid wasps that exhibit several G. agilis.OffspringsexratiosinyoungG. proximus overlapping traits and which co-occur in the same mothers were female-biased and marginally male- small-scale habitats. Gelis agilis, G. proximus and biased in G. hortensis. As mothers aged, however, the G. hortensis are abundant in meadows and forest edge ratio of male:female progeny produced rapidly in- habitats in the Netherlands. Gelis agilis is asexual (all creased until no daughters emerged later in life. Our female), whereas the other two species reproduce sexu- results reveal significant differences in reproductive ally. Here they developed on cocoons of the primary traits among the three species despite them co- parasitoid Cotesia glomerata.Whenprovidedwithun- occurring in the same microhabitats, being very closely limited hosts, lifetime reproductive success was three related and morphologically similar. The increase in the production of male progeny by Gelis mothers over time suggests a depletion in sperm number or viability with J. A. Harvey (*) Department of Ecological Science, Section Animal Ecology, VU age. This is especially interesting, given that Gelis spe- University Amsterdam, Amsterdam the Netherlands cies are among the least fecund parasitoids thus far e-mail: [email protected] studied. It is likely that in the field most Gelis mothers are probably only able to parasitize a few hosts and to J. A. Harvey : L. de Haan Department of Terrestrial Ecology, Netherlands Institute of maintain the production of female offspring. Ecology, Droevendaalsesteeg 10 6708 PB Wageningen The Netherlands Keywords Realized lifetime fecundity. Longevity. O. Verdeny-Vilalta Gelis . Hymenoptera . Secondary parasitoids Ynsect, Rue Pierre Fontaine 1 Évry France B. Visser Evolutionary Ecology and Genetics Group, Biodiversity Research Introduction Centre, Earth and Life Institute, UC Louvain, Croix du Sud 4 1348 Louvain-la-Neuve Belgium Phylogeny and phylogenetic constraints are central to R. Gols our understanding of ecology and evolutionary biology Laboratory of Entomology, Wageningen University, (McKitrick 1993). Phylogeny describes the evolution- Droevendaalsesteeg 1 6708 PB Wageningen The Netherlands ary history and ecophysiological relationships among 244 J Insect Behav (2019) 32:243–251 groups of organisms (Gould, 1977; Nei and Kumar reproductive capacity by a difficulty in finding many 2000). In nature, closely related species generally ex- food plants and therefore invests more metabolic re- hibit traits that very strongly reflect their phylogeny, sources in maintenance than in egg production, allowing such as morphology, reproduction and development it to extend its lifespan in searching for suitable plants on (Cheverud et al. 1985;Blombergetal.2003). Conse- which to oviposit. quently, closely related species generally exhibit a suite Parasitic wasps, or ‘parasitoids’, are model organ- of traits that overlap and which are functionally special- isms for addressing a range of questions in evolutionary ized (West-Eberhard, 1986). Phylogenetic constraints biology. Parasitoids lay their eggs inside or on the bod- are defined as components or aspects of a lineage that ies of other arthropods (‘hosts’) and their larvae grow prevent or impede any anticipated form of evolution in and develop by feeding on host tissues, whereas the that lineage (McKitrick 1993). In other words, a con- adult stage is free-living (Godfray 1994). The develop- straint affects the potential of a species to evolve radical ment of parasitoid offspring is dependent on resources changes in its biology and/or ecology from its ancestors contained in a single host: because hosts of many para- and close relatives and may hinder a species attempting sitoids are only marginally bigger than the parasitoid to exploit novel resources or colonize novel habitats. For itself, they are under intense selection to optimize the instance, in many families of the Hymenoptera exploitation of limited resources to vital metabolic func- (Aculeata) the ovipositor, which is a specialized egg- tions (Harvey 2005; Jervis et al. 2008). By contrast, laying apparatus, has evolved into a stinger that instead selection for resource allocation to different metabolic of eggs injects venom into potential prey or as a means functions in arthropod predators is generally much more of defense against attackers (Zhao et al. 2015). A stinger relaxed, because they are not restricted to a single prey is of much more utility than an ovipositor for a social item. For this reason, parasitoids exhibit a suite of traits wasp, because the workers are sterile and do not repro- that are adapted for exploiting a narrow range of host duce. In vertebrates, woodpeckers possess sharp, point- species in nature, whereas most predators will attack ed bills for chiseling wood for nest construction and many prey species in order to reach maturity. foraging, and long, barbed tongues made up of cartilage Parasitoids that are closely related and/or exhibit and bone for catching insects embedded in trees (Bock similar host ranges in nature often exhibit a convergence 1999;Zhouetal.2009). These adaptations are specifi- in traits such as host utilization and reproduction (Jervis cally tailored for nesting in forest habitats and would et al. 2008). This is because of both phylogenetic con- clearly be of little utility in grasslands. servatism and overlapping selection pressures on trade- Phylogeny is not the only factor constraining organ- offs such as between maintenance and egg production. isms in nature. All species are also constrained in their One of the best examples on how host ecology drives ability to allocate limited metabolic resources for vital similarities and differences in parasitoid traits is a study functions such as reproduction, foraging and survival by Price (1972), who compared parasitoids attacking (Roff 2002). Under strong selection for the acquisition, different stages of the Jack pine sawfly, Neodiprion utilization and allocation of these resources to different swaineii. He found that parasitoids attacking early host and potentially competing fitness functions, the optimal stages, such as young larvae, exhibited traits such as the phenotype of most organisms is determined by trade- production of large numbers of small eggs that could be offs in life-history traits such as between reproduction oviposited rapidly and adults that had short lifespans. and longevity (van Noordwijk and de Jong 1986). A By contrast, parasitoids attacking older hosts, such as trade-off occurs when two fitness-related traits are lim- pupae, produced small numbers of large eggs that took a ited by the same resource, such as time and/or energy, considerable time to lay and adults that had extended that can only be utilized once (Stearns 1989). For ex- lifespans. He attributed these differences to variation in ample, an organism that invests a disproportionate mortality risks experienced by hosts along their ontoge- amount of metabolic resources towards early reproduc- netic continuum with high fecundity being an adaptive tion will invariably experience a reduction in its life response in parasitoids attacking comparatively abun- expectancy and vice-versa. Trade-offs strongly reflect dant young hosts with high mortality risks, and lower environmental limitations on food, prey, mates and other fecundity for parasitoids attacking scarce older hosts factors. Thus, a specialized herbivore that feeds on a rare with a lower mortality risks (Price 1972; see also or small species of plant may be limited in its Pexton and Mayhew 2002). Differences in reproductive J Insect Behav (2019) 32:243–251 245 investment and longevity also appear to reflect host of primary parasitoids (Cotesia spp.) in the field (Lei abundance (Price 1972). and Hanski 1997; van Nouhuys and Hanski 2000; Sex determination in parasitoids is haplodiploid, Harvey et al. 2014; Heinen and Harvey 2019). Thus where unfertilized (haploid) eggs develop into males far 280 species of Gelis have been described (Catalogue and fertilized (diploid) eggs develop into females. This of Life, 2019), although there are certainly many more gives females the choice of deciding what sex to lay as the genus is not well-studied. during oviposition. In parasitoids, numerous studies We compared fecundity schedules, lifetime reproduc- have shown that mothers prefer to oviposit daughters tive success and offspring sex ratios in the three Gelis on larger hosts of perceived higher quality, and sons on species when reared on cocoons of the gregarious
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