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REVIEW article

Front. Ecol. Evol., 08 January 2019
Sec. Behavioral and Evolutionary Ecology
This article is part of the Research Topic Multimodal Mating Signals: Evolution, Genetics and Physiological Background View all 10 articles

The Role of Learning on Insect and Spider Sexual Behaviors, Sexual Trait Evolution, and Speciation

  • 1Department of Biological Sciences, National University of Singapore, Singapore, Singapore
  • 2Yale-NUS College, Singapore, Singapore
  • 3Evolutionary Ecology and Genetics Group, Biodiversity Research Center, Earth and Life Institute, UCLouvain, Louvain-la-Neuve, Belgium

We review experimental and theoretical evidence that learning in insects and spiders affects the expression of mate preferences and of sexual signals, the evolution of both traits, and ultimately patterns of assortative mating, and speciation. Both males and females can modify their sexual preferences and signaling based on previous social interactions or the experience of visual, olfactory, gustatory, or auditory signals. Learning takes place during an early life exposure, previous personal sexual experiences or by observing the choices of others, and it can occur sometimes via very short (a few seconds) exposures to individuals or signals. We briefly review some of the molecular mechanisms that mediate learning in insects, as well as theoretical work that assesses how learning impacts the evolution of insect sexual traits and speciation. We suggest that future research should attempt to provide evidence of the adaptive nature of learning, which remains scarce in insects as well as in vertebrates, and explore further the mechanisms of learning in order to probe into their possible transgenerational inheritance. Future studies should also model how this process might further affect the evolution of sexual traits, and provide a unifying terminology for the underlying mechanisms of learning across diverse life-history contexts.

Introduction

Sexual behaviors such as the expression of a mate preference or the expression of a sexual signal are often not fixed but can be modified through social experience in both vertebrates and invertebrates. This leads to animals learning a mate preference or learning to display a sexual signal such as a courtship dance or the release of a pheromone blend. Learning sexual behaviors has been accepted for quite some time in mammals and birds, where most research has been conducted (Hebets and Sullivan-Beckers, 2010; Verzijden et al., 2012; Morand-Ferron and Quinn, 2015; Servedio, 2015; Head et al., 2016), including early work by Konrad Lorenz on learned sexual preferences via imprinting. However, learning in sexual selection remained controversial for insects and other arthropods until recently (Dukas, 2006, 2008a). This stems from insects being thought of as having fixed sexual behaviors due to their short lives and few mating opportunities, limiting their possibilities for learning or its likely adaptive value. However, a large number of more recent studies have illustrated that both insects and spiders modify their behavioral sexual interactions upon previous experience. Furthermore, it is now abundantly clear that many species of insects mate multiply, and have complex brain structures allowing short and long term memory of previous experiences that impact their lifetime mating behavior (Dukas, 2006, 2008a; Chittka and Niven, 2009).

The effect of social experiences, or simply the exposure to a sexual signal such as a pheromone, on the expression of mate preferences and sexual signals has been described in different terms by different authors (Tables 1, 2), from “learning” and “courtship conditioning,” to “mate copying,” to “exposure,” to “premating interaction,” “social learning,” “experience,” “eavesdropping,” “mate preference learning,” and “learned mate recognition,” among a few. This diverse terminology reflects a burgeoning field for insects and spiders over the last decade, as well as the diversity of learning mechanisms that may be at work in these animals. Regardless of terminology (Table 3), what all these cases have in common is a significant change in the expression of mating behaviors that results from a prior social experience or previous exposure to a sexual signal.

TABLE 1
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Table 1. A non-exhaustive list of publications about how male insects and spiders learn sexual behaviors.

TABLE 2
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Table 2. A non-exhaustive list of publications about how female insects and spiders learn sexual behaviors.

TABLE 3
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Table 3. Summary of the different types of learning in sexual selection in insects and spiders. Modified from (Yeh and Servedio, 2015) and (Varela et al., 2018).

Our goals in this review are to: (1) highlight the multiple types of information that insects learn that later result in changes in their mating preferences or in the expression of their sexual signals; (2) propose a systematic categorization of the underlying learning mechanisms, by building on a framework developed in vertebrates (Table 3); (3) review some of the molecular mechanisms underlying the learning process; (4) review some of the relevant mathematical models, originally applied to vertebrates, that suggest that learning mechanisms have consequences to the evolution of sexual traits and reproductive isolation in insects and spiders. We end by suggesting opportunities for future research in this field.

Insects and Spiders Learn a Variety of Social Information and Signals That Impact Their Mating Behavior

Learning in the context of mating has been described in a large diversity of spider and insect species (Tables 1, 2). Multiple definitions of learning were used across disciplines, but here, we define learning broadly as being a change in the future sexual behavior of an individual resulting from a previous social experience (Thorpe, 1963; Barron et al., 2015). This definition encompasses all described processes of learning (Table 3), for which the adaptive value of the changed behavior has usually not been demonstrated. Learning often involves changes to mating preferences or to speed of sexual response in females, while it usually involves changes in the level of expression of sexual signals in males. In the majority of investigated cases, and perhaps contrary to what is often assumed, naïve females often do not develop a sexual preference until they are exposed to other members of their species or of closely related species (Figure 1A). The absence of a naïve preference appears to be especially common for visual sexual signals, which have been the topic of most research. However, when an innate sexual preference is observed, females can also modify it (Figure 1B) or become more selective (narrow their preference regarding potential mates) (Figure 1C). In males, learning can lead to changes in the courtship intensity, latency to court, target of courtship, or sometimes the expression of the sexual signals.

FIGURE 1
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Figure 1. Illustration of how learning can affect a mate preference function. All graphs describe the mate preference of an individual to increasing amount of a sexual signal. (A) Individuals “acquire a preference” when they do not have an innate preference, but acquire one through experience. (B) Individuals “shift their preference” if they have an innate preference for one signal which is changed to another one after experiencing it. (C) A “change of selectivity” involves other types of modifications of the mate preference function, which depends on the individual responsiveness, tolerance and strength of response to a continuously distributed trait. Details on the measure of selectivity can be found in Fowler-Finn and Rodríguez (2012a,b) [Figure adapted from Fowler-Finn and Rodríguez (2012b)].

Most experimental evidence of learning in altering sexual behavior in insects comes from early exposure of sexually immature adults to the phenotypes of surrounding individuals, what has been called “sexual imprinting” in vertebrates. However, sexual behaviors can also vary after the observation of the interaction between other mating individuals, such as in cases of mate-choice copying (e.g., Mery et al., 2009) or imitation of sexual signaling (e.g., Clark et al., 2012, 2015), or from previous sexual interactions with or without mating (Tables 13). Most studies do not demonstrate that male or female behavioral shifts have an adaptive value, but such value is often assumed. Below, we illustrate this growing experimental evidence of learning in arthropods organized by the type of learned information: social information with unidentified individual signals (when the full phenotype of the interacting individuals is provided to the “learner”), or of specific signals such as olfactory, tactile, visual, and acoustic including vibratory signals (see Tables 1, 2 for a more complete overview, Figure 2).

FIGURE 2
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Figure 2. Illustrations of learning sexual traits or preferences in insects and spiders. Learning can produce an acquisition or a shift of preference, or a change in the insect selectivity for the sexual signal. These processes can be due to mate choice or sexual signaling copying or to sensitization, which is an increase of the individual attraction to the stimuli upon exposure. All examples illustrate changes in the mate preference function, except for the courtship behavior copying, which illustrates a change in sexual signaling.

Social Exposure Without Clearly Identified Learned Signals

Authors report that a social experience, with or without mating, affects subsequent sexual interactions of focal individuals. In most of these studies, adults are exposed to the full phenotype of other individuals where the specific assessed and learned signal(s) are not clearly identified. For example, virgin female crickets reared in isolation approach and contact males less frequently than virgin females reared in a group (Tinghitella, 2014). Being housed with groups of males or females induces fruitless knockout Drosophila males, which have lost their ability to court, to recover their courtship behavior, and wild type males to reduce their same-sex sexual behaviors (Bailey et al., 2013; Pan and Baker, 2014). Burrow-digging spider males enlarged their burrows upon rejections by females, which increases their chances of mating, as females prefer larger burrows (Carballo et al., 2017).

The mating status or novelty of the interacting individuals appears to be particularly important in modifying a focal individual's subsequent behavior. For instance, naive female crickets and spiders are more likely to mate, copulate more quickly or cannibalize fewer males than their mated counterparts (Johnson, 2005; Wilder and Rypstra, 2008; Judge et al., 2010). Male fruit flies learn to focus their courtship toward receptive conspecific females, and out-compete sexually inexperienced males, based on previous copulations (Saleem et al., 2014), or based on rejections by mated or virgin females (Dukas, 2005; Ejima et al., 2005; Griffith and Ejima, 2009). These males also learn from rejections from heterospecific females (Dukas, 2004, 2006, 2008b, 2009; Kujtan and Dukas, 2009; Dukas and Dukas, 2012; Dukas and Baxter, 2014) or immature males (Gailey et al., 1982; McRobert and Tompkins, 1988; Bretman et al., 2010). Learning to quickly discriminate receptive from unreceptive individuals is likely adaptive as males can reduce the costs of unsuccessful courting and mating with an unreceptive female or a male. Females in many species also prefer a new male over their previous mate. For instance, in crickets (Bateman, 1998), in moths (Xu and Wang, 2009; Li et al., 2014), in hide beetles (Archer and Elgar, 1999), or in female Drosophila melanogaster, a simple exposure without mating is enough to trigger a similar preference for a new male (Odeen and Moray, 2008; Loyau et al., 2012). This type of learning might also be adaptive as by rejecting the males that they saw copulating, females could reduce the costs of mating with semen-limited males (Loyau et al., 2012).

Visual Signals

Multiple studies have shown that naïve individuals have no innate genetic mate preferences for particular visual signals but develop these through learning. In many cases, naïve males direct their courtship toward a wide range of females, while inexperienced females display no preference for a specific male visual trait. For instance, male fruit flies, who initially court both large and small females with equal vigor, will preferentially court one of these female types if previously exposed or mated to them (Balaban-Feld and Valone, 2017). In wolf spiders, juvenile or adult exposure to male tibia types is necessary to limit the female preference to a specific leg tuft size or color (Hebets, 2003, 2007; Rutledge et al., 2010; Stoffer and Uetz, 2015, 2016a,b). Male damselflies learn to prefer the female color morphs they previously interacted with (Miller and Fincke, 1999, 2004; van Gossum et al., 2001; Fincke et al., 2007; Takahashi and Watanabe, 2010b, 2011). Experienced female damselflies learn to reject heterospecific males by recognizing their wing patches (Svensson et al., 2010, 2014; Verzijden and Svensson, 2016). The acquisition of a preference for visual traits has also been reported in fruit flies [eye color, (Verzijden et al., 2015)], butterflies [hindwing ornamentation number, (Westerman et al., 2014)], or crickets [size, (Bateman et al., 2001)] (Figure 2). Recent studies on mate-choice copying showed that virgin individuals tend to prefer male phenotypes with similar color type and ornamentation as the mate choice of another conspecific, e.g., in spiders, (Fowler-Finn et al., 2015) and fruit flies, (Mery et al., 2009; Nöbel et al., 2018a). These cases illustrate that insects can generalize socially learned public information for choosing a mate. Finally, male spiders can also copy the leg-tapping dance of other courting males to increase their likelihood of seducing a female (Clark et al., 2012, 2015; Figure 2). These males reach copulation more quickly and are less likely to be cannibalized (Sullivan-Beckers and Hebets, 2011, 2014).

In the few documented cases of insects displaying innate (naïve) visual signal preferences, learning can be context dependent, and sometimes may override, or even reverse these preferences. For instance, female Bicyclus anynana butterflies can switch their naive preference from males with two UV-reflective spots on their forewings to four spots if they are exposed to these males shortly during sexual maturation Westerman et al. (2012). Importantly, learning is context dependent, as female butterflies learn to avoid, rather than prefer, the novel wing patterns when the male sex pheromone is absent in the training male (Westerman and Monteiro, 2013). This suggests that olfactory communication may trump visual communication in assessing mates, at least in B. anynana butterflies. In addition, learning can be biased in that some sexual signals (supernumerous eyespots) can induce an increased preference while exposure to others (fewer eyespots) does not modify innate mate preferences (Westerman et al., 2012).

Olfactory Signals

In multiple studies, the learned sexual signal that triggers a behavioral change is an olfactory signal. Innate preferences appear to be generally present for olfactory signals in insects, and they can trigger a wide range of behaviors in receivers of many species from the same or the opposite gender. Odor learning can lead to either habituation or to sensitization, which led to opposite behavioral responses, but it is still unclear how the two processes work. Already ~35 years ago, studies reported how male sweat bees avoided mating with previous mates, or with females genetically close to their first mate, by learning to recognize their particular odor (Barrows, 1975; Smith, 1983; Wcislo, 1987). Similar processes were recently reported in rove beetles and fruit flies (Schlechter-Helas et al., 2012; Tan et al., 2013). Such “habituation” to female odor also occurs in male moths, which reduce their level of response to female sex pheromones shortly after exposure to components of the blend (e.g., Robledo et al., 2018; Suckling et al., 2018). On the contrary, increased behavioral sensitivity to sex pheromones, termed “sensitization,” was also described in Spodoptera littoralis moths whereby sexually mature adult males increase their responsiveness and attraction to the odor source 24 h after exposure (Anderson et al., 2003, 2007; Silvegren et al., 2005). Male S. littoralis also learned to prefer a mating site based on a learned plant odor, and reproduced preferentially with females found on the same plant where they grew up as larvae, or on plants where they previously mated (Anderson et al., 2013; Thöming et al., 2013; Proffit et al., 2015). Female B. anynana butterflies not only become sensitized to wild-type male sex pheromone composition, but can also learn to prefer unattractive blends if exposed to these blends during sexual maturation, right after adult emergence (Dion et al., 2017; Figure 2). Female moths also perceive the sex pheromone of other females, which induce them to emit their own sex pheromone earlier and at higher amount than inexperienced individuals (Stelinski et al., 2006; Sadek et al., 2012). Finally, the presence of antiaphrodisiacs, transferred by males onto the female cuticle, and reproductive tract led other males to learn to avoid mated Drosophila females (Ejima et al., 2005, 2007).

Acoustic Signals

Multiple studies have shown a change in sexual behavior upon exposure to acoustic signals, which are often used in species recognition and mate quality assessment in insects (Hedwig, 2016). For example, the rate and number of male calls that female crickets hear as juveniles or during mating significantly affects their preference and their response speed to future mate calls (Wagner et al., 2001; Rebar et al., 2011; Kasumovic et al., 2012). Contrary to individuals exposed to a mixture of call frequencies, females reared in silence respond faster toward a model song mimicking the populations' average calling rate (Bailey and Zuk, 2008, 2009; Bailey and Macleod, 2014; Swanger and Zuk, 2015). Males reared in silence intercept more females attracted to other males' calls and increase their own call rates (Bailey et al., 2010). Changes in a females' response to acoustic experience are variable and population-specific (Bailey and Zuk, 2012). The acoustic environment also impacts female treehopper's preference selectivity (Figure 1C) for male signal frequency and speed (Fowler-Finn and Rodríguez, 2012a,b; Rebar and Rodriguez, 2016; Fowler-Finn et al., 2017). In addition, naïve female Drosophila initially show no preference to the courtship songs (wing vibrations) of conspecific or heterospecific males, but a pre-exposure to conspecific songs makes them prefer this song type (Li et al., 2018). In some parasitoid wasp species, males identify host pupae parasitized by a conspecific using acoustic and vibratory signals, learn their location, and visit them regularly, as a strategy to attain prospective emerging female mates (Danci et al., 2013, 2014). This is one of the few cases where the adaptive value of learning is highlighted.

Molecular Mechanisms of Learning

As detailed above, insects can change their sexual preferences and signaling upon social experiences and exposure to a variety of visual, odor, gustatory, or auditory signals, indicating that sexual behaviors are not fixed but plastic. The underlying molecular mechanisms that control this plasticity, however, are still largely unclear. Below we review a few mechanisms mediating such neural system plasticity.

A social learning experience, such as courtship conditioning, where males experience female rejection in response to courtship, can lead to long-term changes in the behavior of males. This process of long-term memory consolidation in male Drosophila appears to depend on a peak of the ecdysteroid hormone, 20E, that appears immediately after the conditioning (Ishimoto et al., 2009).

Insects can learn to prefer (or avoid) a novel visual signal in a mate via early exposure to that signal but mechanisms of plasticity for preference development have only been explored in a non-sexual context. For instance, mRNA of three opsin genes in worker casts of the ant Camponotus rufipes increased upon exposure of these ants to daylight, as did volume of the three subneuropils of the optic lobe (including lamina, medulla, and lobula) (Yilmaz et al., 2016). A specific increase in UV and green opsin mRNA was also observed in the moth Helicoverpa armigera in response to 6 h exposure to UV light (Yan et al., 2014). These examples suggest that exposure of insects to particular visual signals displayed by the opposite sex could lead to changes in specific opsin expression levels as well as structural changes in the optic lobe, increasing sensitivity to those signals, and perhaps leading to later changes in sexual behaviors and preferences. This remains however to be investigated. Changes in protein expression levels and in cell size, cell number and cell connectivity of higher brain compartments in response to details of color patterns or courtship steps, rather than mere exposure to light of different colors, are also likely taking place but mediating mechanisms are still not known.

Mechanisms of pheromone odor sensitization have been explored to some extent in Spodoptera moths. In these experiments males are being briefly pre-exposed to a scent plume containing one or more components of the pheromone blend that increased their sensitization to the odor relative to naïve males (Anderson et al., 2003). The mechanisms that mediate this sensitization involve increases of the specific olfactory receptor expression and odor binding proteins in the antennae a few hours after the exposure (Wan et al., 2015), increased firing responses of the antennae (López et al., 2017) and of the odor receptor neurons (Guerrieri et al., 2012), as well as changes in the size of the neural compartment processing the pheromone components in the olfactory lobes (Guerrieri et al., 2012). These physiological and structural changes have been hypothesized to lead to long-term memory of the early odor experience and stable changes in behavior (Anderson et al., 2007; Guerrieri et al., 2012).

Males learn to recognize mated or heterospecific Drosophila females thanks to the presence of cuticular hydrocarbons and antiaphrodisiacs transferred by the previous male onto the female's cuticle and reproductive tract (Ejima et al., 2005; Billeter et al., 2009). Recent work has identified neuronal differences across Drosophila species that are responsible for species-specific mate preferences regarding a female cuticular pheromone sensed by the legs of males (Seeholzer et al., 2018). It is possible that this conserved neuronal circuit, which is activated differently across species, is plastic and will be later implicated in learning of novel cuticular pheromones within a species, but this remains to be tested.

Drosophila males produce courtship songs by vibrating their wings. The song frequencies are perceived by the tip of the antennae, which detects air particle oscillations, and are processed by the Johnston's organ, at the base of the antennae (Ishikawa and Kamikouchi, 2016). The mechanisms that mediate the female's development of a song preference are still largely unknown but they involve signaling via the main inhibitory neurotransmitter, gamma-Aminobutyric acid (GABA), acting on the GABAA receptor Rdl in specific neurons (Li et al., 2018).

Currently there is limited evidence that learned mate preferences can be transmitted to the next generation in an insect and even more limited understanding regarding mechanisms. Daughters of B. anynana females exposed to novel sex pheromone blends show naïve preferences similar to those of their exposed mothers and different from non-exposed naïve individuals (Dion et al., 2017), but the mechanisms mediating the inheritance of this learned preference are unknown. Prolonged (5 day) olfactory conditioning in Drosophila was also inherited across two generations, but this work did not test the role of these learned odors on sexual behaviors (Williams, 2016).

Mathematical Models Show That Learning Has an Evolutionary Impact

In this section, we first briefly introduce models that assess whether learning itself can evolve and be selected as an evolutionary stable strategy (ESS), i.e., a strategy that if adopted by a population in a given environment cannot be invaded by any alternative strategy that is initially rare. If learning sexual traits is an ESS, then this implies that learning sexual traits is adaptive. Whether learning sexual traits affects their evolution and impacts speciation has also mostly been addressed with theoretical models that we also reviewed in this section.

The first set of models reveal that learning can be selected as an ESS, which is a prerequisite for learning to affect the evolution of sexual signals, mate preferences, and reproductive isolation (reviewed in Galef and Laland, 2005; Vakirtzis, 2011; Verzijden et al., 2012; Dukas, 2013; Servedio and Dukas, 2013; Witte et al., 2015; Head et al., 2016; Kopp et al., 2018; Varela et al., 2018). Overall, for learning to evolve under selection there needs to be genetic variation for learning ability within a species (Mery and Kawecki, 2005). This appears to be the case. An example involves the “rover” and “sitter” alleles at the foraging locus of D. melanogaster that confer different learning abilities to fly larvae when foraging for food (Mery et al., 2007; Papaj and Snell-Rood, 2007; Mery, 2013).

The second set of models assess whether learning affects the evolution of sexual traits and impacts speciation. These models were originally designed for sexual interactions in vertebrates, but here we focused on those models that can be applied to insects (Supplementary Table 1). Most of these models were built on the premise that sexual signals and mate preferences have a genetic basis (e.g., Ritchie, 2000; Shaw, 2000; Noor et al., 2001) that can be modified and be overridden by learning (Supplementary Table 1). The models usually focus on one of the following three underlying mechanisms of learning: “learning by sexual imprinting,” “learning by copying,” and “learning from previous experience” (Table 3 and Supplementary Table 1).

The first group of models focused on imprinting, which occurs when juveniles up to a certain age can learn a sexual preference by observing the phenotypes of surrounding adults (Immelmann, 1975; Head et al., 2016). In insects, the terms “early experience,” or “early exposure” to other individuals of the same generation are used instead of “imprinting” (Table 3). This is primarily because there is still no data on whether or not insects have a fixed period in development or early adulthood when they can learn a preference from a social experience, as in the case of birds, where the term imprinting was first used (Lorenz, 1935). In insects, sexual imprinting of mate preferences can occur between genetically unrelated individuals of the previous or of the same generation, and is termed oblique or horizontal imprinting, respectively (Table 3). Oblique or horizontal imprinting have limited effect on the evolution of sexual preferences and of reproductive isolation, except when spatial structure is taken into account. Spatial structure in models assumes that social learning is only possible between individuals that can perceive each other (Yeh and Servedio, 2015), i.e., that are close in space. Differentiation in social interactions between populations due to spatial isolation is expected to accelerate divergence of sexual preferences, signals, and of reproductive isolation between populations, through coupling of the divergent sexual signals and mate preferences across space (Bailey and Moore, 2012). If populations are exchanging migrants, oblique imprinting of mate preferences cannot produce sympatric speciation (Verzijden et al., 2007), and the populations cannot maintain genetic differentiation in their sexual traits (Yeh and Servedio, 2015). Interestingly, aversive learning of mate preference through oblique imprinting, when individuals learn to avoid a phenotype, was shown to accelerate reproductive isolation and to produce adaptive radiations (Gilman and Kozak, 2015). Finally, imprinting may contribute to reproductive isolation in insects through self-imprinting (i.e., self-referent phenotype matching) that facilitates reinforcement between incipient divergent lineages (Servedio et al., 2009).

Imprinting can also affect the expression of sexual signals, and these learned signals can also contribute to reproductive isolation (Williams and Slater, 1990; Ellers and Slabbekoorn, 2003; Lachlan and Servedio, 2004; Olofsson and Servedio, 2008; Olofsson et al., 2011; Planqué et al., 2014). These models often incorporate a spatial structure, but it is unclear if they can be applicable to insects because they assume that males learn to produce their sexual signals by imitating adults surrounding them during their development, which has so far has been documented only in the wolf spider Schizocosa ocreata (Clark et al., 2012, 2015). These models also assume that assortative mating takes place between females and males that have learned to prefer, or express, a similar sexual signal by experiencing it locally, while assortative mating based on similarly preferred and expressed sexual traits does not occur in insects, as far as we know.

A second mechanism of learning sexual behaviors in insects is to copy another individual's mating decision. Insects that mate in groups, such as promiscuous or lekking species [e.g., some species of ants, bees, paper wasps, and butterflies (Litte, 1979; Wickman and Jansson, 1997; Velthuis et al., 2005; Izzo and Tibbetts, 2012; Prato and Soares, 2013)] can modify their mating preference or the production of their own sexual signals by observing the success of other individuals mating. Most work has focused on “mate choice copying” (“MCC” hereafter), which is usually modeled as “positive” such that individuals (usually females) learn to prefer the phenotype of males that they have observed mating earlier (Servedio and Kirkpatrick, 1996; Santos et al., 2017). The copying behavior itself can spread in a population both through direct (Dugatkin and Höglund, 1995; Stöhr, 1998) or indirect (Servedio and Kirkpatrick, 1996; Santos et al., 2017) selection. MCC has direct selective benefits, if it reduces the sampling costs and/or the error rate of mate choice (Dugatkin and Höglund, 1995; Stöhr, 1998; Agrawal, 2001), but also has indirect selective benefits (Kirkpatrick and Dugatkin, 1994; Servedio and Kirkpatrick, 1996; Santos et al., 2017). These indirect benefits arise because females that copy others are more likely to mate with males that are attractive to other females, spreading in the process genes for attractive sons and genes for daughters with the ability to copy others. MCC can also both increase the variance in male sexual signals (Wade and Pruett-Jones, 1990), and erode genetic variance by eliminating novel or rare male signals, even if these males are fitter than the common males in the population (Kirkpatrick and Dugatkin, 1994). However, when biases in learning are present in mate choice copying, such that females are more strongly affected by experiences involving unusual stimuli (e.g., rare male phenotypes) than those involving standard stimuli (e.g., common male phenotypes), MCC can cause novel male signals to sweep through the population even if there is no inherent preference for the novel trait (Agrawal, 2001). Invasion of a novel sexual signal can also occur when “negative” MCC (aversive learning) is modeled, where females learn to avoid males avoided by other females (Santos et al., 2014). While Kirkpatrick and Dugatkin (1994) suggest that MCC may promote or accelerate population divergence, the role of MCC in reproductive isolation and speciation remains an open question (Varela et al., 2018).

A third learning mechanism occurs through previous (so-called “private” or “personal”) experiences of either courtship or of actual mating events, during which mate preferences and the expression of sexual signals can be learned (Servedio and Dukas, 2013; Morier-Genoud and Kawecki, 2015). Females learning to prefer local or familiar (previously encountered) males increases the rate of divergence between spatially structured populations (Bailey and Moore, 2012), and also in case of a secondary contact (Servedio and Dukas, 2013). In contrast, when males learn to prefer local or familiar females, population divergence can be reduced because competition for accessing these females increases. Heterospecific males, which seldom meet heterospecific females locally, don't learn to prefer them as much as conspecific males, and keep courting and mating with both types of females (Servedio and Dukas, 2013). When males learn to improve the expression of their sexual signals through repeated courtship events, this accelerates the evolution of the sexual signal, even when the signal is costly, and it favors the emergence and spread of a novel male sexual signal, even in the presence of gene flow (Morier-Genoud and Kawecki, 2015).

Finally, some models compared the fitness advantage, or the likelihood of various mechanisms of mate preference learning to spread as evolutionary stable strategies (ESS). Learned mate preferences from previous encounters with potential mates increase fitness compared to other mate selection mechanisms including threshold-based mate preference (Dubois et al., 2012). Furthermore, the advantage provided by learning increases when variance in the quality among males increases locally, and across space or time (Collins et al., 2006). Depending on associated costs, learning mate preferences either through MCC or through previous personal experience can both coexist as an ESS in mixed populations of females displaying either one or the other learning mechanisms (Dubois et al., 2012).

Conclusions and Perspectives

Experimental work on the role of learning in sexual interactions in insects and spiders is a burgeoning field revealing that the traditional view that insects are small robots with mostly innate, genetically fixed sexual behaviors, is now obsolete. Learning in sexual interactions is the rule rather than the exception in every organism tested so far. Innate, genetically fixed sexual preferences and signals are present only in some species, and are more commonly observed in specific modes of communication such as olfactory signals, whereas learning a sexual preference or the expression of a sexual signal is widespread. Learning also affects the expression of innate sexual traits. Learning is usually assumed to be positive, but it can also be negative (i.e., aversive), as well as biased and context-dependent.

Our review revealed the diversity of terminology used by authors to describe experiments involving learning [Table 1, 2, column “Type of learning (as per the authors)”], which can be confusing and prevent the identification of the underlying mechanisms. Hence, we would like to encourage researchers to provide explicit details of their methods as described in Tables 13 (e.g., the developmental stage at which the learning happens, the sex of the demonstrator and of the insects that learns). This information will specify the processes of learning used by insects, e.g., sensitization, simple exposure, or conditioning, which will help identify the underlying neurophysiological mechanisms involved.

Finally, most scientists assume that learning sexual traits has evolved under selection, as appears to be the case in vertebrates (Morand-Ferron, 2017) and regarding other behaviors in insects (Nieberding et al., 2018), but there is little to no evidence that learning sexual traits affects insect fitness, particularly in the wild. This is perhaps because one of the first definition of learning included adaptation [learning is an “adaptive change in individual behavior as the result of experience;” Thorpe (1963)]. We encourage field work to complement laboratory experiments with ecologically-relevant setups to quantify the adaptive value of learned sexual interactions across insects. Showing the adaptive value of such learning would explain its prevailing presence in such miniature brained, short lived, organisms.

Author Contributions

ED, AM, and CN conceived the scope of the review, collected information from the literature, and contributed to the writing and editing of the manuscript. All authors contributed to revisions.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments

The authors thank Maria Servedio for her helpful comments on the mathematical model part of this review, and Astrid Groot and Varvara Vedenina for their invitation to contribute to the special issue. This work was supported by the Ministry of Education, Singapore grants MOE2014-T2-1-146 and MOE2015-T2-2-159 to AM and ED, and by the University of Louvain-la-Neuve (UCL) and the Fédération Wallonie-Bruxelles (Grant ARC 17/22-086) to CN. This is publication BRC 340 of the Biodiversity Research Center at UCL.

Supplementary Material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fevo.2018.00225/full#supplementary-material

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Keywords: mate choice, preference, selectivity, signal, social experience, adaptive value, sexual selection

Citation: Dion E, Monteiro A and Nieberding CM (2019) The Role of Learning on Insect and Spider Sexual Behaviors, Sexual Trait Evolution, and Speciation. Front. Ecol. Evol. 6:225. doi: 10.3389/fevo.2018.00225

Received: 01 August 2018; Accepted: 05 December 2018;
Published: 08 January 2019.

Edited by:

Astrid T. Groot, University of Amsterdam, Netherlands

Reviewed by:

Valentina Zizzari, Universität Koblenz Landau, Germany
Matthew R. E. Symonds, Deakin University, Australia

Copyright © 2019 Dion, Monteiro and Nieberding. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Emilie Dion, dion.emilie@ymail.com
Antónia Monteiro, antonia.monteiro@nus.edu.sg
Caroline M. Nieberding, caroline.nieberding@uclouvain.be

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