Pheromone Blend Does not Explain Old Male Mating Advantage in a Butterfly

Abstract

In several insect species, male mating success is higher in older than in younger males, although condition diminishes dramatically with age. Two hypotheses are under debate to explain the counterintuitive pattern of old male mating advantage: first, an increased eagerness of older males to mate, driven by their low residual reproductive value, and second female preference for older males based on chemical cues such as sex pheromones (female choice hypothesis). In a series of experiments, we manipulated female olfaction, male pheromone blend and female age to test whether old male mating advantage prevails when the influence of male sex pheromones is controlled for, using the tropical butterfly Bicyclus anynana as model. We found that older males had a higher mating success than younger ones irrespective of female scent-sensitivity and irrespective of male pheromone blend. Interestingly, older males were found to court more often and for longer time bouts than younger males. These results were independent of female age, although younger males courted younger females more often and for longer bouts than older females. Taken together, our results indicate that male courtship activity (1) is higher in older compared to younger males and (2) increases the mating success of older males. Olfaction and sensing pheromones, in contrast, were not a necessary prerequisite for old male mating advantage to occur and may use other cues than pheromones to assess male quality.

Old male sex: large ejaculate, many sperm, but few offspring

“…The lower ejaculate quality of older males is clearly evidenced by pronounced detrimental effects on female reproduction. As in B. anynana older males were previously found to have a much higher mating success than younger males (Fischer et al 2008;Kehl et al 2014), these findings support the notion that old male mating advantage here arises from sexual conflict rather than female preference for older males . Given the rather strong fitness reductions in females having mated with older males reported here, it seems difficult to imagine that potential indirect genetic benefits would be able to compensate for the negative effects.…”

“…from a higher eagerness and persistence of older males during courtship rather than female preference for older males. This notion is supported by the fact that older males show higher flight activity and court more frequently and for longer time bouts than younger males, while females having mated with older males show a shorter refractory period, a higher remating propensity, and suffer reduced egg-hatching success than females having mated with younger males (Fischer et al 2008;Kehl et al 2014). The latter suggests that older males transfer a spermatophore of lower quality to females, either in terms of reduced nutrients, sperm viability, or sperm numbers, as found in other insects (Kaitala and Wiklund 1995;Wedell and Ritchie 2004).…”

“…Older males of this species have been described as having a higher mating success than younger ones Kehl et al 2014). However, several lines of evidence suggest that old male mating advantage arises from sexual conflict, i.e.…”

Dense, small and male-biased cages exacerbate male–male competition and reduce female choosiness in Bicyclus anynana

“…Yet, other research in B. anynana supports the hypothesis that male behaviour (male sexual harassment, male competition) may be a stronger determinant of mating outcome than female choice, as evidenced by male courtship persistence and aggressiveness in 'latching onto the female's abdomen to copulate' (e.g. Fischer et al, 2008;Geister & Fischer, 2007;Janowitz & Fischer, 2010, 2012Kehl et al, 2014). We suggest that our results provide an explanation for this seemingly opposite pattern regarding the relative importance of female choice versus male courtship activity on mating outcome across B. anynana mating experiments.…”

The erroneous courtship hypothesis: do insects really engage in aerial wars of attrition?

“…Based on the erroneous courtship model, we can understand these results as older males having a smaller j because they have less residual reproductive value, and so persist longer. In line with this notion, older males of the butterfly Bicyclus anynana tend to court females more earnestly than do younger males (Fischer, Perlick & Galetz, 2008;Kehl et al, 2014).…”