Loser in Fight but Winner in Love: How Does Inter-Male Competition Determine the Pattern and Outcome of Courtship in Cricket Gryllus bimaculatus?

Abstract

Animal females are generally assumed to prefer males that win fights. However, a growing number of studies in numerous animal taxa demonstrate no correlation between male fighting ability and their attractiveness, or even female preferences for fight losers. One of the methods to measure female preferences employs no-choice tests that evaluate a female's latency to mating when placed with a single male. Considering that courtship behavior generally contains multimodal signaling, we analyzed 19 behavioral elements demonstrated by both sexes of the cricket Gryllus bimaculatus during courtship. To estimate male dominance status, males were preliminarily tested in two rounds of fights. Females mounted males with different fighting ability equally often, but the latencies from the start of antennal contact to mount were shorter in fight losers than fight winners. During courtship, males with high fighting ability demonstrated one of the elements of agonistic display, rocking the body, more frequently, and for longer durations than males with low fighting ability. This element was negatively correlated with singing in fight winners but was positively correlated with singing a courtship song in fight losers. Rocking is thereby suggested to have multiple signaling functions in agonistic and courtship behavior. The song parameters were poorly related with male mating success. Fight winners, rather than fight losers, tended to produce a higher number of calling chirps, which could be explained by the inability of males with high fighting ability to quickly shift from aggression to courtship behavior. The results suggest that increased aggression in fight winners is likely to interfere with subsequent courtship.

Evolutionary dynamics of sex-biased genes expressed in cricket brains and gonads

“…bimaculatus exhibits aggressive male-male fighting and mate guarding [42,43] and males transfer larger spermatophores to females when in the company of rival males [44]. Such behaviors are likely mediated by the male brain.…”

“…We suggest here that several features of the mating biology of G. bimaculatus might cause episodic adaptive evolution and underlie the high dN/dS values observed herein (see also below section "3.7 Evidence of A History of Positive Selection in Sex-Biased Gonadal and Brain Genes"). For instance, G. bimaculatus exhibits aggressive male-male fighting and mate guarding (Vedenina & Shestakov, 2018;Gee, 2019) and males transfer larger spermatophores to females when in the company of rival males (Lyons & Barnard, 2006). Such behaviors are likely mediated by the male brain.…”

“…Moreover, many aspects of its mating biology are currently well understood. G. bimaculatus exhibits intense male-male and sperm competition, including aggressive male-male fighting and mate guarding (Vedenina & Shestakov, 2018, Gee, 2019), increased rates of male transfer of spermatophores to females in the presence of other males (Lyons & Barnard, 2006), and the complete mixing of sperm from multiple males in the storage organ of the female reproductive tract, the spermathecae (Morrow & Gage, 2001, Simmons, 1986). In addition, females have shown preferences for novel and young mating partners (Zhemchuzhnikov et al, 2017), and for males with larger body size and higher quality auditory signals (Zhemchuzhnikov et al, 2017, Bateman et al, 2001).…”

Male competition reverses female preference for male chemical cues

“…Results of female preference can then be compared between females given males with and without a competition context. Social context extends beyond the immediate surrounding behavioral phenotypes to include the past experiences of social partners (Filice & Dukas, 2019;Hsu & Wolf, 1999;Oliveira et al, 2009;Vedenina & Shestakov, 2018). Previous interactions can perpetuate dominant/subordinate relationships, and ultimately affect who has access to mates (Hsu & Wolf, 1999;Oliveira et al, 2009Oliveira et al, , 2011.…”

Toward Testing for Multimodal Perception of Mating Signals

“…In both these examples, signal variants in single vs. combined modalities result in different behavioral reactions of receivers (Narins et al, 2005;Bretman et al, 2011). A closer look at other taxonomic groups shows more examples: Many species of birds show complex, rhythmic visual displays during singing (Williams, 2001;Dalziell et al, 2013;Ullrich et al, 2016), fish grunt and quiver (Estramil et al, 2014;de Jong et al, 2018), spiders and grasshoppers have visual-vibratory courtship displays (Stafstrom and Hebets, 2013;Kozak and Uetz, 2016;Vedenina and Shestakov, 2018), and some Process through which multimodal cues or signals (in communication) are grouped by the brain to belonging to one object or being one signal…”