Identification of seminal proteins related to the inhibition of mate searching in female crickets

Abstract

In response to the reduction in fitness associated with sperm competition, males are expected to evolve tactics that hinder female remating. For example, females often display a postmating reduction in their sexual receptivity that has been shown to be mediated by proteins contained in a male’s seminal fluid (sfps). However, although there has been comprehensive research on sfps in genetically well-characterized species, few nonmodel species have been studied in such detail. We initially confirm that female Australian field crickets, Teleogryllus oceanicus, do display a significant reduction in their mate-searching behavior 24 h after mating. This effect was still apparent 3 days after mating but was entirely absent after 1 week. We then attempted to identify the sfps that might play a role in inducing this behavioral response. We identified two proteins, ToSfp022 and ToSfp011, that were associated with the alteration in female postmating behavior. The knockdown of both proteins resulted in mated females that displayed a significant increase in their mate-searching behaviors compared with females mated to males having the full compliment of seminal fluid proteins in their ejaculate. Our results indicate that the female refractory period in T. oceanicus likely reflects a sperm competition avoidance tactic by males, achieved through the action of male seminal fluid proteins.

Males adjust their manipulation of female remating in response to sperm competition risk

“…Further, males are believed to strategically allocate resources into the production of sfps. Male T. oceanicus upregulate the expression of a collection of sfps when experiencing sperm competition risk [33], including those previously found to inhibit female mate searching behaviour (ToSfp022 and ToSfp011) [10]. Therefore, we suggest that it is this socially cued modulation in sfp allocation that probably induced the variability in female mate searching observed here.…”

“…They are involved in a vast array of functions including regulating sperm storage and forming mating plugs as well as influencing many female physiological, behavioural and life-history traits [22]. In a number of insect species, including T. oceanicus, male sfps have been demonstrated as the mechanism through which males inhibit female post-mating sexual receptivity [10,[12][13][14]22]. Further, males are believed to strategically allocate resources into the production of sfps.…”

“…In the Australian field cricket, Teleogryllus oceanicus, males are thought to manipulate the remating behaviour of females. Recently mated females engage in significantly less mate searching behaviour [10] and are less responsive to male song [11]. Similar to other insects [12][13][14][15], this post-mating inhibition of female sexual receptivity probably occurs, at least in part, as a function of proteins contained within a male's seminal fluid (sfps) [10].…”

“…When exposed to a risk of sperm competition, males produce ejaculates with greater sperm viability [35]. This corresponds to an increased expression of seven sfp genes [33], including two proteins previously found to influence female remating (ToSfp022 and ToSfp011) [10]. And many of the same genes that are upregulated in response to sperm competition risk are instead downregulated when males experience an increase in sperm competition intensity [34], corresponding to a reduction in sperm viability [36].…”

“…Similar to other insects [12][13][14][15], this post-mating inhibition of female sexual receptivity probably occurs, at least in part, as a function of proteins contained within a male's seminal fluid (sfps) [10]. At least two sfps, ToSfp022 and ToSfp011, appear to play a role in inhibiting female mate searching [10]. Generally, male T. oceanicus suffer a loss in paternity that is proportionate to the number of mates accepted by a female [16,17].…”