Rethinking same-sex sexual behaviour: male field crickets have broad mating filters

Abstract

Same-sex sexual behaviour (SSB) occurs in many animals and is often treated as an anomaly requiring special explanation. One common explanation for SSB is mistaken identity. However, animals make similar ‘mistakes’ in other contexts—such as attempting to mate with immature individuals or inanimate objects. Framing such behaviours as ‘mistakes’ risks misinterpreting how animals make flexible mating decisions. Here we make a case for an alternative approach to thinking about SSB by instead considering an individual's mating filter. A broad filter means directing courtship toward anything that resembles a potential mate, whilst a narrow filter means only courting with receptive targets. We illustrate this approach by examining the mating filters of male Pacific field crickets (Teleogryllus oceanicus). We find that males engage in SSB but also misdirect courtship toward juveniles (but not plastic crickets). This finding suggests that SSB is not an anomaly and is better considered alongside other misdirected behaviours. We argue that by viewing misdirected behaviours through the lens of mating filters rather than as ‘mistakes’ we can build a more nuanced understanding of reproductive behaviour and begin to determine when having a broader mating filter can be advantageous.

1. Introduction

Same-sex sexual behaviour (hereafter SSB)—defined as courtship or mating interactions between members of the same sex—is widespread in the animal kingdom, occurring in a large number of vertebrate and invertebrate species [1–3]. SSB is often framed as an evolutionary paradox or anomaly because it generates no direct reproductive benefits but incurs potential costs, such as time, energy or opportunity costs [3,4]. Various adaptive and non-adaptive hypotheses have been proposed to explain the evolution and maintenance of SSB in animal populations [1,5–10]. For example, in garter snakes, males may attract courtship from other males to warm up faster [11], while female–female pair bonds in the Laysan albatross enable females to achieve reproductive success in female-biased populations [12]. A commonly invoked non-adaptive or proximate explanation for the occurrence of SSB, particularly when observed in insects, is that of mistaken identity—in which individuals target sexual behaviours toward members of the same sex because they mistake them for members of the opposite sex [13–15].

However, there are two main issues with the prevailing view of SSB as an anomaly and with mistaken identity in particular. Firstly, mistaken identity is not unique to SSB. In fact, many similar forms of misdirected sexual behaviour occur in other contexts. For example, animals are known to direct sexual behaviour toward heterospecifics, dead individuals, immature individuals and even inanimate objects [16–18], all of which provide no direct reproductive benefits but incur potential costs. Misdirected behaviour is also not limited to sexual behaviours; behaviours such as aggression and parental care can also be directed toward incorrect targets [19–21]. For example, brood parasitism is a well-studied phenomenon that involves a host misdirecting parental care toward unrelated offspring. So rather than representing an anomaly, SSB may be better considered as just one example of a behaviour being expressed outside of its original function.

Furthermore, by framing SSB and other misdirected behaviours as ‘mistakes,’ we risk misinterpreting how animals make flexible, context-specific decisions about their mating behaviour. Mating decisions are influenced by both the physical and social environment with different conditions favouring different decisions. For example, if appropriate sexual partners are common in the population, and the cost of initial courtship is low, spending a great deal of time and energy discriminating between males and females (or between mature and immature individuals etc.) may not be particularly advantageous. In fact, two recent theoretical models have demonstrated that selection can favour indiscriminate mating under a wide variety of conditions [10,22] with some arguing that indiscriminate mating forms the ancestral condition for sexual organisms [9]. Thus, the expression of misdirected sexual behaviours, including SSB, may be better viewed as a consequence of context-appropriate flexibility in mating behaviour rather than as a ‘mistake’ per se.

Here we suggest that a productive approach would be to place SSB within a broader framework that encompasses other examples of misdirected courtship and avoids labelling such behaviour as ‘mistakes’. We can do this by considering what might be termed an individual's ‘mating filter’, which describes the breadth of stimuli that will elicit sexual behaviours (such as courtship or mounting). For example, a broad mating filter means directing courtship toward anything that resembles a potential sexual partner. By contrast, a narrow mating filter would involve directing sexual behaviour only toward desirable and receptive members of the opposite sex. Mating filters could be asymmetric if, for example, certain stimuli are more important than other for eliciting courtship behaviour. For instance, an individual might only engage in courtship if the stimulus is the right size or has the correct scent. Furthermore, at the neuronal level, individuals may have multiple filters that vary in their broadness to specific parts of signal parameter space, and it is the joint effects of these multiple filters that will determine how an individual responds to a stimulus. We can therefore reframe some of the study of SSB from ‘do individuals engage in SSB and why?’ to ‘do individuals have broad or narrow mating filters and what might cause an individual's mating filter to change?’

This approach draws upon signal detection theory (also called acceptance threshold theory)—a framework originating in psychology [23,24] that has been applied to studies of animal behaviour in a variety of contexts [25–28]. Signal detection theory predicts an optimum level of discrimination based on the costs and likelihood of making an acceptance error (e.g. courting something other than an opposite sex adult) or rejection error (e.g. not courting an opposite sex adult). This idea has also been described in the context of immune responses as the ‘smoke detector principle’ [29]—it is better to have a smoke detector that is extremely sensitive in reacting to a small stimulus rather than one that is overly discriminating, because the cost of a rejection error (i.e. not sounding when there is a fire) is so high. A similar logic extends to mating behaviour. If the costs of rejecting a potential mating opportunity are high, then false alarms (i.e. courting the wrong target) will occur. Under these circumstances, individuals might make several kinds of acceptance errors—not just courting individuals of the same sex, but directing their efforts to other unsuitable targets.

We are not the first to suggest such an approach. Signal detection theory has been previously applied to the study of male SSB in burying beetles [27] and water striders [14]. In burying beetles, when the costs of rejecting females were experimentally increased, males had broader mating filters and showed higher levels of SSB; whereas, when the costs of accepting males increased, males were more discriminating and showed lower levels of SSB [27]. Thus, SSB occurs as a consequence of males adjusting their mating filter based on the fitness costs of rejecting females or accepting males. However, to broaden our understanding of mating behaviour, it is now timely to generalize our approach by examining mating interactions other than just SSB. If individuals engage in other kinds of misdirected sexual behaviour then it would suggest that flexible mating filters are a ubiquitous part of mating behaviour and allow us to begin drawing general patterns between SSB, reproductive interference and other mating interactions. Doing so allows us to place SSB into a broader picture of reproductive behaviour rather than treating its occurrence as an anomaly.

To illustrate a mating filters approach, we experimentally examined misdirected sexual behaviour in male Pacific field crickets (Teleogryllus oceanicus). We exposed males to either females, males, juveniles of either sex, a plastic cricket or no stimulus (control). If male crickets have broad mating filters, they should attempt to court stimuli other than adult females—which would be consistent with the idea that SSB is not different from other examples of misdirected courtship behaviour. On the other hand, if male crickets have narrow mating filters, then only adult females will elicit courtship behaviour.

T. oceanicus is an ideal system to examine mating filters because males produce a distinct courtship song which is easily distinguished from other acoustic signals [30], making it straightforward to record the presence or absence of courtship behaviour. In addition, T. oceanicus exhibit misdirected courtship behaviour; males court and mount other males [13,31] and will court dead females [17]. SSB is more likely if males have previously interacted with a female [13,31], suggesting that cues about the presence of a female may decrease the risk of acceptance errors and trigger males to broaden their mating filter. However, it is unknown whether such effects extend to other kinds of mating interaction such as interactions with juveniles or inanimate objects.

2. Methods

(a) . Cricket stocks and rearing

We used crickets from a large, outbred laboratory population originally derived from eggs laid by wild-caught females from Hilo, Hawaii. This laboratory population is supplemented with eggs from the wild approximately once per year. We housed crickets at consistent densities (approx. 25 adults) in multiple 15 l plastic containers and provided with ad libitum access to rabbit food, moist cotton for water and oviposition and cardboard egg carton for shelter. Crickets were kept in a Caron Insect Growth chamber maintained at 26°C, 75% relative humidity with a photoreversed 12 : 12 light–dark cycle.

We isolated mature adult males (2–4 weeks post eclosion) from the stock population for use in our experiment. We moved each male to an individual 118 ml plastic cup containing food, water and egg carton and maintained them for 3 days prior to testing.

(b) . Treatments

Males were haphazardly assigned to one of six treatments based on the type of stimulus they subsequently interacted with during testing: female, male, juvenile female, juvenile male, a plastic cricket and control.

In the female and male treatments, focal males interacted with adult females or males from the stock population. In the two juvenile treatments, focal males interacted with late instar juveniles from the stock population. To minimize variation in the age and development stage of juveniles we only selected juvenile females that had an ovipositor smaller than 2 mm and juvenile males that had only developed the first pair of wing buds, indicating that they were in the second to last instar. In the plastic cricket treatment focal males interacted with plastic crickets (Ownsig, Shanghai, China) that are the same size as, and bear a superficial resemblance to, adult crickets (electronic supplementary material, figure S1). Finally, focal males in the ‘control’ treatment were kept alone. The purpose of this final treatment was to determine if males ever exhibit courtship behaviour when alone, allowing us to verify that males were likely responding to the test stimuli.

To enable us to distinguish focal males in trials with more than one male we marked the pronotum of focal males in all treatments with a small spot of gold marker paint (Uni POSCA, Mitsubishi Pencil Co., Tokyo, Japan). Marking was performed 1 h before males were used in trials to minimize the likelihood it would affect their behaviour. Previous use of similar marker paints had no discernible effect on behaviour [32].

(c) . Pre-trial

Prior to each trial all males were moved to a clean 118 ml cup with a female from the stock population and left to interact for 10 min. SSB is an infrequent behaviour, but pre-trial exposure to females has been found to increase the incidence of SSB in subsequent male–male trials [13]. We therefore performed pre-trial exposure to females both to increase the likelihood that males engage in misdirected sexual behaviour and to facilitate comparison of our study with previous work [13,31]. We recorded whether males produced courtship song and whether the female mounted the male during the 10 min of pre-trial interaction. Courtship song is a short-range signal that is used to induce females to mount. Courtship song is easily distinguished from other acoustic signals because it includes a long, constant-intensity trill which is distinct from the short chirps that characterize calling song and aggressive ‘victory’ song [30]. If the female mounted the male (females mount males in this species), we gently separated the two using a paintbrush to prevent copulation. A female was only used once in pre-trial treatments, and females used in pre-trial treatments were not used as stimuli in subsequent trials.

(d) . Trials

Immediately after the pre-trial treatment we moved focal males to another clean 118 ml cup containing the appropriate stimulus for their treatment (i.e. a female, a male, a juvenile female, a juvenile male, a plastic cricket or nothing in the case of controls) and observed them for 10 min. During the observations we recorded the presence of courtship, calling and/or aggressive behaviour by focal males. Courtship behaviour was again indicated by the presence/absence of courtship song. Males were scored as calling if they produced calling song that is used to attract females from a distance. Finally, we scored aggressive interactions as present if focal males engaged in stereotypical aggressive behaviours including bouncing, lunging, antennal fencing, biting, chasing or flipping [13,31,33,34]. After trials, males were weighed to the nearest milligram and their pronotum width recorded to the neared 0.01 mm. All behavioural observations were performed in a 22–26°C room under red light.

(e) . Statistical analyses

To determine whether males are more likely to engage in courtship, calling or aggressive behaviour based on the type of stimulus they received, we ran binomial generalized linear models (GLMs) with the presence/absence of courtship, calling or aggression as response variables. Treatment (female, male, juvenile female, juvenile male, plastic cricket or control) was included as a categorical factor. We specified female as the reference level for the model of courtship, control as the reference level for the model of calling, and male as the reference level for the model of aggression. To aid model interpretation we removed treatment levels if no males engaged in a particular behaviour in that treatment group. For example, no males in the control treatment were observed courting or showing aggression so we removed control males from these analyses. Similarly, no males in the female treatment engaged in calling or aggression so we removed the female treatment from these two models. Removing these factor levels from our models had no qualitative effect on the results. To compare between treatment levels, we performed pairwise Tukey post-hoc contrasts using a Bonferroni correction to adjust for multiple testing. We included pre-trial experiences (i.e. whether the male courted the pre-trial female, and whether the pre-trial female mounted the male) as additional factors because males may be more likely to engage in courtship if they have previously courted a female [13,31]. Finally, we included the body mass and pronotum width of focal males as additional covariates to account for differences in condition and/or size that may influence behaviour. All analyses were performed in R (v. 4.1.2; [35]) loaded with the packages lme4 [36], MASS [37], car [38] and multcomp [39]. All data and code are available at https://osf.io/he9m3/?view_only=ab9264c83d4b455c9ea444ba0fefb02a [40].

3. Results

(a) . Courtship

We observed courtship behaviour by focal males in all treatments except for controls (treatments with courtship: female = 27/30; male = 14/30; juvenile male = 19/28; juvenile female = 28/29; plastic cricket = 2/30; control = 0/29). A larger proportion of focal males courted females than courted males (table 1 and figure 1). Focal males were more likely to court juvenile females than they were to court males—but there was no difference in the focal males' propensity to court males and juvenile males (table 1; figure 1). The proportions of focal males that courted juvenile females and juvenile males was comparable to the proportion that courted females (table 1; figure 1). Males were less likely to court plastic crickets than they were to court females, males or juveniles of either sex (table 1; figure 1).

Table 1.

Effect of treatment stimulus (female, male, juvenile female, juvenile male, a plastic cricket, or control), pre-trial courtship (y/n), pre-trial mounting (y/n), focal male body mass (mg) and focal male pronotum width (mm) on the presence of focal male courtship, calling or aggressive behaviour. We provide R², parameter estimates ± standard errors (s.e.), z-values and p-values from binomial generalized linear models. Pairwise comparisons are Tukey post-hoc tests with Bonferroni correction for multiple testing. The treatment on the right in each pair is the reference level for that comparison. For example, a negative estimate for courtship means males were less likely to court the stimulus on the left compared to the stimulus on the right. Significant p-values (after correction) are in bold type. (Note that controls were removed from the models on courtship and aggression and females were removed from the models on calling and aggression to aid convergence. See text for details.)

response	R2	predictor	d.f.	estimate (±s.e.)	z-value	p-value
courtship	0.458	treatment	4
		male versus female		−2.46 (0.78)	−3.15	0.0016
		male versus juvenile female		−3.13 (1.10)	−2.83	0.023
		male versus juvenile male		−0.90 (0.61)	−1.46	0.28
		juvenile female versus female		0.66 (1.24)	0.53	0.59
		juvenile male versus juvenile female		−2.22 (1.13)	−1.96	0.19
		juvenile male versus female		−1.56 (0.811)	−1.93	0.053
		plastic cricket versus female		−5.40 (1.05)	−5.13	< 0.001
		plastic cricket versus male		−2.93 (0.87)	−3.36	0.0053
		plastic cricket versus juvenile female		−6.07 (1.27)	−4.76	<0.001
		plastic cricket versus juvenile male		−3.84 (0.89)	−4.31	<0.001
		pre-trial courtship (y/n)	1	2.93 (1.03)	2.83	0.0045
		pre-trial mounting (y/n)	1	−0.303 (0.64)	−0.47	0.63
		body mass (mg)	1	5.78 (5.53)	1.04	0.29
		pronotum width (mm)	1	0.40 (1.46)	0.27	0.78
calling	0.381	treatment	4
		male versus control		−3.65 (0.91)	−3.99	<0.001
		male versus juvenile female		0.55 (1.11)	0.50	1.00
		male versus juvenile male		−0.31 (0.97)	−0.32	1.00
		juvenile female versus control		−4.21 (1.04)	−4.02	<0.001
		juvenile male versus control		−3.34 (0.85)	−3.91	<0.001
		juvenile male versus juvenile female		0.87 (1.00)	0.86	1.00
		plastic cricket versus control		−4.90 (1.23)	−3.96	<0.001
		plastic cricket versus male		−1.25 (1.30)	−0.95	1.00
		plastic cricket versus juvenile female		−0.69 (1.27)	−0.54	1.00
		plastic cricket versus juvenile male		−1.56 (1.22)	−1.28	1.00
		pre-trial courtship (y/n)	1	3.00	2.10	0.035
		pre-trial mounting (y/n)	1	−0.86	−1.12	0.26
		body mass (mg)	1	8.89	1.41	0.15
		pronotum width (mm)	1	−0.81	−0.55	0.57
aggression	0.187	treatment	3
		juvenile female versus male		−2.45 (0.77)	−3.16	0.0015
		juvenile male versus male		−1.69 (0.64)	−2.62	0.0086
		juvenile male versus juvenile female		0.76 (0.83)	0.91	1.00
		plastic cricket versus male		−2.36 (0.74)	−3.15	0.0016
		plastic cricket versus juvenile female		0.098 (0.87)	0.11	1.00
		plastic cricket versus juvenile male		−0.66 (0.82)	−0.81	1.00
		pre-trial courtship (y/n)	1	−0.024 (0.99)	−0.025	0.98
		pre-trial mounting (y/n)	1	−0.54 (0.59)	−0.19	0.35
		body mass (mg)	1	−7.26 (5.65)	−1.28	0.19
		pronotum width (mm)	1	2.19 (1.46)	1.49	0.13

Figure 1.

Proportion of focal male crickets that produced courtship song when exposed to a female, a male, a juvenile female, a juvenile male, a plastic cricket or nothing (i.e. control). Letters above the bars indicate statistically significant pairwise differences from Tukey tests with Bonferroni correction. Controls were removed from the analysis as no males produced courtship song in this treatment. Numbers inside the bars show the number of trials in which courtship was observed.

Males were more likely to attempt courtship in a trial if they had courted in the pre-trial interaction with a female (table 1). However, the likelihood of courtship behaviour was not influenced by whether males were mounted by pre-trial females (table 1). Finally, male body mass and male pronotum width did not influence the likelihood of courtship (table 1).

(b) . Calling

Calling behaviour was rare in all treatments except for controls (treatments with calling: female = 0/30; male = 2/30; juvenile male = 3/28; juvenile female = 2/29; plastic cricket = 1/30; control = 19/29). A significantly larger proportion of males called in control treatments compared to all other treatments (table 1; figure 2a). Males were more likely to call in a trial if they had courted in the pre-trial interaction with a female (table 1). However, the likelihood of calling behaviour was not influenced by whether males were mounted by pre-trial females, or by the focal male's body mass or pronotum width (table 1).

Figure 2.

Proportion of focal male crickets that either called (a) or acted aggressively (b) when exposed to a female, a male, a juvenile female, a juvenile male, a plastic cricket or nothing (i.e. control). Letters above the bars indicate statistically significant pairwise differences from Tukey tests with Bonferroni correction. Treatment levels where no males were observed calling or acting aggressively were removed from the analysis. Numbers inside the bars show the number of trials in which a given behaviour was observed.

(c) . Aggression

Aggressive behaviour was observed in all treatments except for controls and females (treatments with aggression: female = 0/30; male = 16/30; juvenile male = 5/28; juvenile female = 3/29; plastic cricket = 3/30; control = 0/29). Aggressive behaviour was more common in male–male treatments than other treatments (table 1; figure 2b). The likelihood of aggressive behaviour was not influenced by whether or not males courted pre-trial females or were mounted by pre-trial females (table 1). Focal male body mass and pronotum width did not influence the likelihood of aggression (table 1).

4. Discussion

SSB is often treated as a unique problem in need of a special explanation. However, an alternative view is that SSB is just one of many examples of misdirected behaviour. We argue that the evolution and occurrence of SSB and other misdirected reproductive behaviours can be better understood by considering an individual's mating filter. To illustrate this approach we examined SSB and misdirected courtship in male Pacific field crickets. Males misdirected courtship toward non-reproductive juveniles and (rarely) inanimate objects—suggesting that SSB is not unique from other misdirected behaviours and that continuing to consider SSB as an anomaly is unhelpful. Here, we first discuss our empirical results in the context of mating filters and prior work on SSB. Next, we make a broader case for how a mating filters approach can benefit our understanding of the occurrence and evolution of SSB and other misdirected behaviours.

(a) . Empirical results

Male crickets courted other males, a form of SSB, but also readily courted juveniles (figure 1). Since juveniles are not sexually mature, directing courtship toward them provides males with no immediate fitness benefits. This finding supports the suggestion that SSB is a consequence of having a broad mating filter. Males were just as likely to court juveniles of either sex as they were to court adult females (figure 1), indicating that male mating filters encompass non-reproductive individuals in this species. By contrast, males rarely courted plastic crickets (figure 1), suggesting that a stimulus that is the same size and shape as an adult cricket is not enough to trigger misdirected courtship behaviour in this species. This finding is perhaps unsurprising, as having too broad of a mating filter would likely be costly in terms of time and energy. Nevertheless, this result demonstrates that an additional benefit of a mating filters approach is that is can be used to determine what additional cues (e.g. olfactory cues, movement, etc.) are required before courtship behaviour is misdirected.

Males were more likely to court juvenile females than adult males. One potential explanation for this result is that males can distinguish males from females more readily than they can distinguish between juvenile and adult females. This could occur if males use chemical cues such as cuticular hydrocarbons (CHCs) to identify females. CHCs are contact pheromones found on the exoskeletons of most terrestrial arthropods [41]. However, sexual dimorphism in the CHC profiles of T. oceanicus are not apparent until after adult eclosion and only become exaggerated after sexual maturation [42]. Another possibility is that it is the absence of male CHCs, which are transferred to females during mating, that is the salient cue to males when deciding whether or not to court. Alternatively, the behaviour of juvenile females may make it more likely that males court them than adult males—for example, if juvenile females are less active or aggressive than adult males, then the costs of misdirecting courtship (e.g. time, energy or risk of injury) toward juveniles may be lower than for adult males.

Empirical work in burying beetles (Nicrophorus vespilloides) has shown that males plastically adjust their mating filters in response to changes in either the costs or benefits of accepting or rejecting a mating opportunity [27]. We did not examine plasticity in mating filters in our experiment. However, our results could suggest that other misdirected behaviours, such as courtship toward juveniles, could be similarly context dependent. For example, males may be less likely to misdirect courtship behaviour if they are in poor condition if being in poor condition increases the costs of courtship. We therefore echo Engel et al. [27] in encouraging further empirical work on the extrinsic and intrinsic factors that could influence plastic changes in mating filters in the context of SSB but also more broadly by examining other misdirected behaviours. For instance, examining what factors determine whether individuals court heterospecifics or provide parental care to potentially unrelated offspring would be productive.

(b) . Broader applications of a mating filters approach

A mating filters approach can advance our understanding of misdirected behaviour and has the potential to provide a more nuanced and complete view of variation in reproductive behaviour. Viewing SSB not as an anomaly but as a consequence of a broad mating filter is useful because it groups SSB alongside other forms of misdirected behaviour, such as courtship toward juveniles, heterospecifics or inanimate objects. Doing so allows us to broaden our understanding of the causes and consequences of misdirected behaviour, which is important because misdirected behaviours can have evolutionary consequences. For instance, mating with heterospecifics can weaken reproductive isolation between species and attempting to mate with inanimate objects can lead to evolutionary traps [18,43].

As previously argued, framing SSB as a ‘mistake’ is unhelpful because doing so can lead us to overlook the contexts in which indiscriminate courtship may be advantageous. Having a broad mating filter may allow individuals to make the most of limited opportunities. In other words, courting a same-sex individual (or a juvenile or a heterospecific, etc.) is not necessarily a mistake if having a broad mating filter reduces the risk of missing mating opportunities. This view is supported by recent theoretical work showing indiscriminate mating (which leads to more frequent SSB) is the optimal strategy under a wide range of conditions [10,22]. Thus, we encourage future studies to reconsider labelling the occurrence of SSB as a result of ‘mistaken identity’ and instead describe the broadness of mating filters.

Another benefit of a mating filters approach is that it implicitly encourages us to consider which factors may cause mating filters to shift. Individuals might broaden their mating filters if the costs of rejecting a suitable partner are high (e.g. if searching or discriminating are costly) or if the costs of accepting an unsuitable partner are low (e.g. suitable partners are abundant). Similarly, individuals might switch to narrower filters if conditions favour being more discriminating. There are many factors that could shape these costs and benefits including the population density, the synchrony of receptivity (i.e. are both sexes sexually receptive at the same time), and the sex ratio. For example, male water striders (Tenagogerris euphrosyne) kept in male-biased sex ratios have broader filters (i.e. they engage in more SSB) than males kept in female-biased sex ratios [14]. In addition, individual state might influence mating filters—for instance, if individuals in poor condition pay higher costs of searching, courting or discriminating then we might predict that individuals in poor condition will have narrower mating filters than individuals in good condition. Thus, investigating whether individuals in poor condition are less likely to misdirect behaviour would be an interesting avenue for future work. Mating filters may also vary with respect to the sensory modality used to find or assess potential mates. For example, individuals may have broader filters with respect to signals in one modality (e.g. acoustic) but a narrower filter with respect to others (e.g. olfactory). Finally, sex differences in mating filters could occur if the costs or benefits of accepting or rejecting a partner are larger for one sex than the other. For example, males may be more likely than females to misdirect their sexual behaviour since the costs of an acceptance error are typically larger for females [18]. So far, most work on SSB has focused on males [3,7] perhaps because males are often assumed to be less discriminating in their mating behaviour, but females also misdirect behaviour (e.g. toward heterospecifics; [44]) suggesting that investigating mating filters in females would be another productive avenue for future work.

Finally, a mating filters approach allows us to compare misdirected behaviour across different contexts. For example, do individuals with broad mating filters in the context of SSB also have similarly broad mating filters for heterospecifics? There is some evidence this may be the case as a review of SSB in insects and arachnids found that approximately 20% of publications that reported evidence of SSB also reported evidence of sexual behaviour toward heterospecifics [3]. This supports our suggestion that taking a broader approach to SSB, rather than treating it as an anomaly, can better our understanding of reproductive behaviour. Finally, a mating filters approach allows us to examine if the same factors that shift mating filters in one context have a similar effect in other contexts. For instance, if the costs of rejecting a valid mating are high (e.g. due to high search costs) then individuals should narrow their mating filters. However, it is currently unclear if, under such conditions, individuals would be equally unlikely to engage in SSB and say heterospecific matings (or other misdirected behaviours).

Data accessibility

Data and code are available from OSF at https://osf.io/he9m3/?view_only=ab9264c83d4b455c9ea444ba0fefb02a [40]. The data are provided in the electronic supplementary material [45].

Authors' contributions

J.R.: conceptualization, data curation, formal analysis, investigation, methodology, visualization, writing—original draft; M.Z.: conceptualization, funding acquisition, supervision, writing—review and editing.

All authors gave final approval for publication and agreed to be held accountable for the work performed therein.

Conflict of interest declaration

We declare we have no competing interests.

Funding

This study was supported by the University of Minnesota.