Habituation of mating preferences: a comment on Daniel, Koffinas and Hughes (2019)

Daniel, Koffinas and Hughes [1] (hereafter DKH) reported that the mating preferences of female Trinidadian guppy (a tropical fish) are subject to habituation, a behavioural phenomenon reflecting a widespread form of ancestral learning in the animal kingdom [2,3]. The authors found that when a female was repeatedly exposed to a male with a given colour pattern, the female mating interest for males with a similar pattern decreased as a function of the number of exposures. DKH also showed that this response decrement presents several features of habituation, such as stimulus specificity (the mating response recovers for a male with a different colour pattern), spontaneous recovery (the response recovers if the habituated male is temporarily removed) and dishabituation (responsiveness to the habituated male recovers after exposure to a novel male).

While the study is certainly of interest, because it shows that habituation can affect biologically significant stimuli, we regretfully have to note that DKH have completely overlooked two areas of research whose results are highly relevant for the question addressed in their study and that can help to understand the reported findings.

To begin with, the notion that the sexual interest toward the same partner is subject to habituation is not a new one, rather it is a well-known phenomenon called the ‘Coolidge’ effect [4]. For example, in their pioneering study on sexual ‘satiation’ in rats in the 1950s, Beach & Jordan found a weakening of the copulating behaviour of a male rat during a period of unlimited access to the same receptive female, whereas the sexual response recovered after a period of inactivity [5]. Although initially the reduced sexual responsiveness was not interpreted as an instance of habituation [5,6], subsequent studies [7,8] began to consider the possibility that the reduction in mating behaviour was not accounted for by sexual fatigue or exhaustion, but rather by mechanisms of habituation [9,10]. In the same period, other studies showed that the sexual capacity of a male rat recovered completely when the female partner was changed, thus showing an important characteristic of habituation, namely stimulus specificity [11,12]. A similar pattern of results has been found in the mating behaviour of male sheep [13]. Furthermore, Fisher in his study [12] on rats anecdotally reported that the habituated male may show a renewed interest in a previously mated female if flashing lights and tones are introduced, which retrospectively can be interpreted as an instance of dishabituation.

Although habituation, with sensitization, is often considered to reflect a form of non-associative learning, associative models of habituation have been proposed in which habituation can be context-specific [14]. Accordingly, evidence of context-specific habituation of different responses in non-human and human animals has been reported [15–17]. In agreement with this view, some evidence exists that in mammals the mating response of a habituated male tends to resume if the same female is encountered in a new environment [18].

From this brief, though not exhaustive, literature review, it is evident that in different taxa mating is subject to habituation. However, it must be acknowledged that the study of DKH differs in one important aspect from the above-mentioned ones. Indeed, whereas in studies on the sexual behaviour conducted on non-human animals several decades ago, habituation of mating preference resulted from an active copulatory behaviour, in the study of DKH habituation to the same male partner is observed despite not being allowed to copulate during the exposure phase. In other words, habituation of the mating preference was achieved simply by exposing the female to the visual features (the colour pattern) of the male partner, which was confined in a different space. This result may appear quite surprising because it would seem natural to assume that habituation of primary drives like hunger, thirst and sex is achieved when the organism has the possibility to consume or get in contact with the stimulus of interest, such as food, beverage or a mating partner. So, how is it possible that the simple repeated exposure to a given sexual signal (the male guppy colour pattern in the DKH study) results in habituation of the female mating preference for that stimulus?

The answer can be found in another research area neglected by the authors and addressing the habituation of reinforcer effectiveness (HRE) [19]. As previously mentioned, habituation is typically studied with respect to stimuli that, although alerting, are in fact irrelevant/innocuous for the organism [2] like, for instance, a sudden tactile, acoustic or visual stimulation. These stimuli, when presented, initially elicit an orienting response, which then habituates as exposure to the same stimulus continues [9]. However, as the HRE phenomenon shows, habituation occurs also for biologically significant stimuli, such as primary reinforcers like food or water [20]. Studies on HRE have documented that, during operant conditioning, animals progressively reduce their interest (i.e. the rate of responding) with respect to the reinforcer being consumed (food or water), a decrement that is only partially explained by satiety factors [21]. Rather, it has been proposed that the reinforcer progressively loses its efficacy in sustaining the operant response because during training the animal habituates to the reinforcer's sensory properties [22], which may include gustative, olfactive and visual features. Hence, HRE can play a key role in regulating the animal consummatory response towards a biologically significant stimulus. In support of the HRE hypothesis, it has been shown that, in humans, the rate of operant responding sustained by food decreases with repeated exposure to the reinforcer even when its consumption is prevented during the conditioning phase [23]. Analogous results have been observed in rats working for a light onset reinforcer, which shows that for some animals, a simple non-consumable visual feature can become a motivationally significant stimulus, which is, however, subject to habituation [24]. Crucially, HRE shows the typical signatures of the general habituation phenomenon: stimulus specificity, spontaneous recovery, dishabituation and frequency dependence [19]. It seems therefore very likely that the habituation of mating preferences reported by DKH might be an instance of HRE, in which the female habituated to the sensory properties of the sexual signal, namely to the colour pattern of the male partner. Note that the results reported by the authors parallel those showing habituation and dishabituation of sexual arousal in human females when exposed to erotic materials [25,26].

Finally, we would like to stress the fact that habituation cannot be at the same time the definition of a behavioural phenomenon (i.e. a reduced responsiveness to stimulus repetition), and the explanation of the same phenomenon. Therefore, habituation cannot ‘ … causes a preference for a novel sexual signal’ as claimed by DKH [1, p. 1], because habituation is the reduced preference for a repeated sexual signal, a phenomenon that requires an explanation. Hence, what needs to be explained is why habituation of mating preference is observed, and such explanation can be found in mechanisms of habituation like those, for example, originally proposed by Sokolov [9], Thompson [10] and Wagner [14].

Data accessibility

This article has no additional data.

Authors' contributions

Both C.C. and M.T. wrote the paper.

Competing interests

We declare we have no competing interests.

Funding

We received no funding for this study.