Males choose to keep their heads: Preference for lower risk females in a praying mantid
Introduction
Sexual cannibalism is a co-evolutionary puzzle found in many different taxa: spiders (Andrade, 1996, Schneider, 2014), scorpions (Peretti et al., 1999), and praying mantids (Kynaston et al., 1994, Maxwell, 1999a). Females of sexually cannibalistic species are known for their voracity during mating, since they may consume their mates either before, during or after the sexual encounter. The costs and benefits of sexual cannibalism for each sex depend on its timing. Sexual cannibalism before copulation can only benefit the cannibalistic female, while sexual cannibalism during or after sperm transfer can benefit both the female and male (Elgar and Schneider, 2004), depending on the future mating opportunities for the male and the effect his consumption has on the production of offspring (Andrade, 1996, Barry et al., 2008, Johnson, 2001).
There are different (although not mutually exclusive) hypotheses that may explain sexual cannibalism. Non-adaptive hypotheses include the aggressive spillover hypothesis (Arnqvist and Henriksson, 1997), which suggests that sexual cannibalism may have evolved as a by-product of selection for high and non-discriminate aggression in the juvenile stage, when aggressiveness results favorable in the foraging context. The mate choice hypothesis (Elgar and Nash, 1988), on the other hand, suggests that sexual cannibalism is an extreme form of mate choice, where females copulate with high quality or preferred males and cannibalize lower quality males before fertilization. The life-history strategy hypothesis (Schneider and Elgar, 2002) states that sexual cannibalism may be a side effect of an increased foraging vigor of females that mature at a smaller size and body mass.
When cannibalism occurs during or after sperm transfer females obtain clear benefits from the consumption of a mate-turned-into-prey: they not only procure the sperm to fertilize their eggs, but they also get a meal in the process. From the males’ perspective, the costs outweigh the benefits in many species (but see Andrade, 1996), since becoming their partner’s meal translates into null future reproductive success. As a result, males have evolved counter-adaptations such as risk avoidance behaviors (Barry et al., 2009, Fromhage and Schneider, 2004, Lelito and Brown, 2006, Maxwell et al., 2010). In turn, risk avoidance behaviors can favour the evolution of new techniques for females to lure males (Barry, 2015), creating an ‘arms race’ between the sexes.
In praying mantids, the behaviors that reduce the risk of cannibalism include slow approaches of males towards females, which can take from several minutes to hours (Lelito and Brown, 2006, Maxwell, 1999b, Prokop and Václav, 2005, Scardamaglia et al., 2015); males freezing upon sight of a female in order to avoid detection (Barry et al., 2009, Lawrence, 1992, Roeder, 1935) and avoiding mating with hungry (Lelito and Brown, 2006, Maxwell et al., 2010) or aggressive (Brown et al., 2012, Scardamaglia et al., 2015) females.
The balance between costs and benefits for males (and thus male behavior) may vary due to factors such as accessibility to sexual partners throughout life: males that experience a higher encounter rate with females are more cautious than those that experience a low mate encounter rate (Brown et al., 2012). In the same way, males approach females more cautiously at the beginning than at the end of the season, in association with the risk of cannibalism: mantids that mature earlier are bigger and more cannibalistic than those that mature later in the season (Prokop and Václav, 2008). Evidence suggests that female cannibalism depends on females’ energetic state: the hungrier the female the higher the probability of sexual cannibalism (Barry et al., 2008, Maxwell et al., 2010), and that males may use female activity or environmental cues to predict the risk of cannibalism (Gemeno and Claramunt, 2006, Scardamaglia et al., 2015). Gemeno and Claramunt (2006), for example, found that Mantis religiosa males approach females more quickly when they capture a prey item. In the same line, Scardamaglia et al. (2015) found that Parastagmatoptera tessellata males may cue on the female predatory strike and avoid aggressive and thus riskier females. In this work, we examined male behavior in response to potential indicators of the risk of cannibalism in praying mantids that occur in the province of Buenos Aires, Argentina. We presented P. tessellata males with three different options in a laboratory-controlled experiment: one female that was observed whilst consuming a prey (hereafter ‘female with prey’), one female that did not get access to a prey (hereafter ‘female without prey’), and a male that was observed consuming a prey (control for the presence of prey, hereafter ‘control male’). Specifically, we studied whether males are sensitive to cues that provide information on female energetic state and whether they show risk avoidance behavior. Contrary to Gemeno and Claramunt (2006), we presented the options simultaneously rather than focusing on male behavior when presenting the options independently. The current experimental design has the advantage of allowing males to choose between females, providing direct evidence of their preference. We hypothesized that males would behave so as to reduce their risk of being cannibalized and we predicted that they would prefer females they had seen consuming a prey recently.
Section snippets
Collection and rearing
The praying mantids were raised in the laboratory from oothecae collected from wild populations in Buenos Aires province, Argentina. Oothecae were incubated at 27–31 °C until egg hatching, which occurred after 24–45 days. Nymphs were reared individually in 150 ml plastic containers during the first three or four instars and then transferred to 450 ml plastic containers. Wooden sticks were placed inside the rearing containers, providing a substrate for perching. Mantids were fed Drosophila
Mating attempts
Mating attempts were observed in 89% (16/18) of the trials. Sixty-nine percent of the mating attempts (11/16) were directed to the female with prey, while 28% (5/16) were directed to the female without prey. None of the focal males attempted to mate with the control male. Focal males did not approach or attempted to mate with any of the individuals during the time of prey ingestion. The mean latency to a mating attempt was 144 ± 23 min (N = 16). Males attempted to mate more frequently with the
Discussion
Male praying mantids (P. tessellata) preferred females that had recently fed on a prey, the option that can potentially reduce cannibalism, when confronted with three different options in choice tests carried out in a controlled laboratory environment. Whether under natural conditions the consumption of a single prey decreases males’ chances of survival may depend on many factors (such as previous female condition and prey size). However, there is no doubt that if the consumption of a prey has
Acknowledgments
L.P. is Researcher at CONICET (Consejo Nacional de Investigaciones Científicas y Técnicas). This work was supported by the Agencia Nacional de Promoción Científica y Tecnológica and the Universidad de Buenos Aires. R.C.S. was supported by an undergraduate fellowship from the Universidad of Buenos Aires. We would like to thank Daniel Campioni for help with preparation of Fig. 1.
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Present address: Instituto de Investigaciones en Producción Animal (INPA-CONICET-UBA), Facultad de Ciencias Veterinarias, Argentina.