An alternative reproductive tactic: A parasitoid wasp gathers and guards a harem by pheromone-tagging virgins
Highlights
► Males of the egg parasitoid wasp Ooencyrtus kuvanae exhibit a harem-gathering and guarding (HGG) mating tactic. ► HGG males pheromone-tag untagged virgins for their harem, then return and mate them. ► Tagged females avoid mating with all males, except for the one that tagged them. ► Females do not incur direct fitness costs by mating with multiply-mated males. ► Specimen-specific tagging-pheromone mediates mate recognition and mate assessment.
Introduction
Alternative reproductive tactics (ARTs) are the expression of two or more ways by which competing males – or sometimes competing females – obtain copulations. ARTs occur frequently in insect mating systems with intense sexual selection (Taborsky et al., 2008, Roff, 2011), are often heritable, and may or may not result in equal fitness (Taborsky et al., 2008).
Similar to a conditional strategy (Gross, 1996), ARTs are primarily condition- and status-dependent (Taborsky et al., 2008). When condition-dependent with such conditions as intense male–male competition over many receptive females within a discrete patch (Emlen and Oring, 1977, Alcock, 1978, Thornhill and Alcock, 1983, Shuster, 2010), or status-dependent when a male's competitive ability is greater than his rivals’ (Gross, 1996), male insects are expected to adjust their alternative male phenotype traits. These phenotype traits may be expressed as different mating tactics (Brockmann and Penn, 1992, Brockmann, 2002, Shuster and Wade, 2003). Such mating tactics include female defense polygyny whereby males prevent others from gaining access to a female (Emlen and Oring, 1977), scramble competition (Brockmann, 2008), or mate searching (Alcock and Buchmann, 2011).
In many parasitoid mating systems, males likely implement ARTs because females often (i) emerge protandrously from a discrete patch (spatially clustered), (ii) are receptive upon emergence, (iii) mate once in their lifetime, and (iv) outnumber males 2:1 (Godfray, 1994, Quicke, 1997, Godfray and Cook, 1997). For example, when receptive females are spatially clustered and synchronously receptive, males choosing a harem gathering and guarding (HGG) tactic could increase the number of receptive females available to them because search time and distance to locate females are minimized (Shuster and Wade, 2003); if males choose to implement an HGG tactic under these conditions, they should be able to deliver sperm to many females (Roitberg et al., 2001, Boivin et al., 2005). Extensive spatial clustering of receptive females also increases female encounter rates for males, and therefore may select for another ART to persist. For example, less competitive males might decide to choose a mate-at-once (MAO) tactic with any female they encounter; MAO males may have lower fitness than HGG males but may still be reproductively successful (Brown et al., 1997, Shuster and Wade, 2003).
Male ARTs can also be affected by female choice (Brockmann, 2008). In a female-defense polygynous mating system, the females’ mate choice may help shape the males’ ART and be based on indirect criteria such as choosing the male that has secured most of the females (Thornhill and Alcock, 1983, Wiley and Poston, 1996).
Parasitoid males may secure females without aggression (van den Assem et al., 1980), even though aggression and weaponry tend to evolve when females are spatially clustered and asynchronously receptive, as in Muscidifurax spp. (van den Assem et al., 1980, Thornhill and Alcock, 1983). When parasitoid females are spatially clustered and synchronously receptive, weaponry is less conspicuous (Shuster and Wade, 2003) and competition may be less aggressive, taking the form of display threats as in Nasonia vitripennis Ashmead (King et al., 1969), contests of speed and agility as in Tetrastichus atriclavus Waterston (van den Assem et al., 1980), or in absentia mate guarding as in Spalangia endius Walker (King and Fischer, 2005).
Males guard mates in absentia through volatile or non-volatile short-range pheromones (Greenfield, 1981, Delisle et al., 2000, Ayasse et al., 2001). Such pheromones may be transferred primarily through antennation, a key behavior exhibited by parasitoids during courtship and/or mating. Antennae are sexually dimorphic (van Baaren et al., 1999), house sex pheromone glands (Isidoro and Bin, 1995, Bin et al., 1999, Steiner et al., 2010) or pheromone receptors (Quicke, 1997, van Baaren et al., 2007), and differ in the number, shape, and type of sensory sensilla (Chapman, 1982), contingent on their function.
Males compete for a positional advantage to release pheromones that (i) counteract attractants associated with receptive females, (ii) convey discreet courtship messages understood only by females of their choice (Thornhill and Alcock, 1983), or (iii) quickly place females into a receptive state.
Life history traits of the egg parasitoid wasp Ooencyrtus kuvanae (Howard) (Hymenoptera: Encyrtidae) are conducive to the coexistence of several male ARTs (Thornhill and Alcock, 1983, Shuster and Wade, 2003, Gross, 1996). This quasi-gregarious, 2 mm wasp parasitizes eggs of gypsy moth, Lymantria dispar dispar L. Female wasps insert a single egg into each accessible egg of a host egg mass that measures 2–3 cm across and contains several hundred eggs covered in setae (Brown, 1984). By fertilizing an egg, female insects produce a daughter, and by not fertilizing it, they produce a son. Within 4 weeks, wasps complete development inside host eggs and emerge en masse as sexually mature adults that can live 4–6 weeks. Females emerge up to 1 day later, are immediately receptive to mating, and are twice as numerous as their brothers. However, a male-biased sex ratio can occur among non-siblings due to local mate competition (Somjee et al., 2011) and because males typically remain on the host egg mass as long as there are mating opportunities, whereas mated females disperse within 24 h, seeking new gypsy moth egg masses (Brown, 1984). Females mate only once in their lifetime shortly after emergence, whereas males mate multiply in their lifetime. Mate attraction is mediated by close-range pheromone components (Ablard et al., 2012). When a male encounters a single female, a stereotypic sequence of events ensues consisting of a brief (ca. 4 s) pre-copulatory ritual, copulation, and a post-copulatory ritual, which may last 15–67 s. Both rituals are mediated by tactile signalling (Ablard et al., 2011).
Our objectives were to explore the presence of ARTs in O. kuvanae. We hypothesized that (1) at least two male ARTs (HGG and MAO) coexist when males are competing over spatially clustered receptive females, (2) one tactic provides more mating opportunities than another tactic, (3) females indirectly choose males, (4) tactics are condition- and status-dependent, and that (5) females do not incur a fitness cost as a result of these tactics.
Section snippets
General protocol
A colony of O. kuvanae was started with specimens field collected near the town of North East, Maryland (39°36′N, 75°55′W) (USA). All insects were reared under a 16:8 h light:dark regime at 22–25 °C and 50–70% relative humidity (RH) (Hofstetter and Raffa, 1997) in the Global Forest Quarantine Facility of Simon Fraser University on eggs of gypsy moth supplied by the U.S. Forest Service (Hamden, CT, USA). They were contained in Plexiglass cages (40 cm × 40 cm × 30 cm) and provisioned with cotton wicks (1 cm
Mating behavior of males in a non-competitive setting
Males courted and mated at once each single female (experiment 1a: binomial test proportion 0.50, n = 15, p < 0.0001) and each female in groups of five (experiment 1b: binomial test proportion 0.50, n = 15, p < 0.0001). In experiments 1a and 1b, the courting and mating sequence were consistent and entailed a brief (ca. 4 s) pre-copulatory ritual, copulation, and a post-copulatory ritual which lasted between 15 and 67 s. All females alone or in groups readily mated with the male.
Mating behavior of males in a competitive setting
Males placed in a
Discussion
In a non-competitive setting, O. kuvanae males invariably and immediately mated any untagged female they encountered (MAO tactic), whether or not she was on her own or in a group. Conversely, under the conditions of a competitive setting, males mostly exhibited two reproductive tactics, a harem-gathering and -guarding (HGG) tactic and a mate-at-once (MAO) tactic, the former yielding a higher fitness. The HGG tactic of O. kuvanae males was not only based on the condition of a competitive
Conclusion
Experimental manipulation of courting wasps enabled us to explore and address some of the theories and outstanding questions about ARTs in insect mating systems including, but not limited to, the functional design of traits related to sexual interactions, such as courtship behavior and pheromones that affect male or female control (Alexander et al., 1997, Johansson and Jones, 2007). In the mating system of O. kuvanae, competing males deploy ARTs and exhibit traits in the early phase of
Acknowledgments
We thank H. Bottomley, P. Cepeda, G. Andersen, M. Andersen, J. Punnett, U. Somjee, S. McCann, Z. Jumean, S. Takács, and S. Bohlke for technical assistance; J. Drummond for ESEM imaging; M. Hrabar for focus-stacked images; R. Ydenberg, B. Crespi, E. Kiehlmann, A. Harestad, C. Lowenberger, J.H. Borden and J. Brockmann for comments on the manuscript; M. Loughin for statistical modelling; and S. DeMuth for graphical illustrations. This work was supported by the Natural Sciences and Engineering
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