Promiscuous words

Promiscuity is frequently used to describe animal mating behaviour, and especially to describe multiple mating by females. Yet this use of the term is incorrect, perhaps reflecting an erroneous adoption of common language to pique reader interest. We evaluated the patterns of use and misuse of the word ‘promiscuity’ in a representative journal of animal behaviour. This survey highlights how inappropriately the term is used, and how it can conceal critical features of animal mating strategies with intriguing evolutionary significance. Further analysis of the scientific impact of papers identified by the term promiscuous or polyandrous revealed that the former were cited less frequently. We argue that using promiscuity to describe animal mating strategies is anthropomorphic, inaccurate, and potentially misleading. Consistent with other biological disciplines, the word promiscuity should be used to describe indiscriminate mating behaviour only, and that polygyny and polyandry should be used to describe male and female mating frequency respectively.


Introduction
Promiscuity is frequently, but largely incorrectly used to describe animal mating behaviour, perhaps reflecting an erroneous adoption of common language to pique reader interest. According to The Oxford English Dictionary, promiscuous originally referred to repeated, indiscriminate actions: "That is without discrimination or method: confusedly mingled, indiscriminate (1605) … Of an agent or agency: making no distinctions: undiscriminating (1633) … casual, carelessly irregular (1837)" [1]. Promiscuity was used to describe human sexual activity in the 19 th Century, the essence (and costs) of which are colourfully observed in George Sala's bawdy pantomime Harlequin Prince Cherrytop (1879): "Better frig, howe'er the mind it shocks, than from promiscuous … [fornication] … catch the pox" [2].
The term 'promiscuity' sneaked into the lexicon of evolutionary biology last century, particularly to describe mating behaviour e.g. [3][4][5][6] and is now widely entrenched (a Web of Knowledge (Thomson Reuters) search for 'promiscu*' , limited to the fields of 'Evolutionary Biology' , 'Zoology' , 'Behavioural Sciences' , and 'Ecology' returned over 700 publications). It is currently typically, although not exclusively [7], applied to describe female multiple mating or polyandrythe latter taking precedent [8].
Science often borrows words from common language: very early uses of the word promiscuous referred to surgical procedures [9], the use of barbiturates [10] and landscape management [11], and more recently molecular biologists use promiscuous to describe certain enzymes [12], gene regulators [13] and receptors [14] as promiscuous, precisely due to their non-specific nature. The use of these terms as scientific jargon draws on the general meaning of the word to highlight indiscriminating processes. This contrasts with its use as a descriptor for multiple mating behaviour, because the implied indiscriminating mate selection process is broadly wrong.
Females are rarely promiscuous, in the general meaning noted in the Oxford English Dictionary: the overwhelming evidence from diverse taxa confirms Darwin's suggestion [15] that females are typically circumspect about their mates [16], accruing a variety of benefits from their discriminate mating [17,18], including with multiple partners [19]. In general, we expect females to remain choosy, irrespective of the number of mating partners, the exception being species in which there is cryptic female choice e.g. [20].
Promiscuous has been used as an umbrella term to include polyandry, polygyny, and polygynandry [21]. While it may be useful to use a single term to describe mating strategies in which males and females mate multiply (arguably, the modal animal mating behaviour), promiscuous is unhelpful because it conflates both the nature (discriminating or not) and frequency of mating. In contrast, the terms monogamy, polygyny, polyandry and polygynandry   Calculated as the number of papers retrieved by the search terms promiscuity or promiscuous, divided by the sum of the number of papers retrieved by the search terms promiscuity, promiscuous and polyandry or polyandrous.
refer to frequency only. We highlight this issue by evaluating the patterns of use and misuse in the scientific literature of the word 'promiscuity' to describe female mating strategies.

Use and misuse of promiscuous
We investigated whether polyandrous females were simultaneously described as promiscuous and exhibiting discriminating mate choice in papers published in a representative journal, Animal Behaviour. Drawing on papers published in the period 2000-2010, we identified those that contained 'promiscuous' (and its associated derivations) in either the abstract or main text. For each paper, we asked to which sex the term was applied (male, female or both), and whether the term was applied in a species in which pre-copulatory female choice had been experimentally demonstrated (either in the article itself or other published papers), or whether the authors inferred or suggested its presence in that species. Female mate choice is typically understood to mean a mating preference for different kinds of males [7,15,16], and is inferred from experiments or field observations showing that females prefer males according to the degree of exaggeration of secondary sexual characteristics e.g. [16][17][18]. We reduced the likelihood of misinterpretation of each paper by ensuring it was assessed independently by at least two readers. We confined our analysis to the term promiscuous because other descriptors of animal mating behaviour (such as polygynous, polyandrous and polygynandrous) do not make inferences about the nature of matingwhether either sex is discriminating or notand thus are not at issue. In total, 39 papers were evaluated (see Table 1). 'Promiscuous' was applied to females in 23 cases, males in 2, and in 14 cases the term was either applied to both sexes or the focal sex was ambiguous (significantly, such ambiguity is impossible with precise language, such as polyandry and polygyny). For papers in which 'promiscuous' was applied to females or both sexes (37 papers), female choice was demonstrated or suggested by the authors themselves in 18 instances, while in 15 cases there was no published evidence of female choice (four cases were excluded as the papers were theoretical reviews or metaanalyses). So, in over half of the instances, promiscuous is evidently used incorrectly, a proportion that is likely to be substantially underestimated: the absence of evidence of female choice in the remaining cases is not evidence that female preferences are absent.
Using promiscuity to titillate the reader?
Promiscuity as a term to describe animal mating behaviour is undoubtedly anthropomorphic, probably accounting for the frequency of its use, especially amongst the primate literature. The discipline does not tolerate other anthropomorphisms in biological science; for example, the term forced copulation is preferred over rape [22], and infanticide preferred over murder [23]. Promiscuity has pejorative and androcentric connotations [20] and is likely to be emotionally evocative [24], typically saved for the females of the species (Table 1): while polygynous males maximise their fitness by mating at the highest rate, females are described as promiscuous. Perhaps promiscuous is used in titles and abstracts precisely because it is titillating, the notion of indiscriminate mating tapping into latent social taboos.
We explored the potential motivation for and consequences of using the term promiscuous by evaluating the citation metrics for papers retrieved by searches in Web of Knowledge (Thomson Reuters). We selected 15 journals and conducted two searches for each journal, using the terms (i) promiscuous OR promiscuity, and (ii) polyandrous OR polyandry (summarised in Table 2). We make the comparison with polyandry only because our previous analysis indicated that, in the vast majority of cases, promiscuity is used to describe female mating frequency (Table 1). Polygyny is widely understood to mean, based on the Greek etymology, multiple mating by males [24] and thus refers to an entirely different behaviour. Roughly a third of the papers included in the sample were identified by the term promiscuous or promiscuity in the title, abstract or key words. While this proportion ranged from 20-50% between journals, it was not correlated with the journal's Impact Factor (Figure 1). Nevertheless, the mean number of citations of 'polyandry' papers (34 ± 7) per journal was marginally greater than that of 'promiscuity' papers (26 ± 4; Wilcoxon Sign-Rank test: p = 0.07), and the single-publication h-index of 'polyandry' papers (16 ± 2) was significantly higher than that of 'promiscuity' papers (9 ± 2; Wilcoxon Sign-Rank test: p < 0.0001) ( Table 2). It is not clear whether this reflects an author's publishing Figure 1 The proportion of 'promiscuity' papers in a journal was not associated with its Impact Factor (2012 Journal Citation Reports, Thomson Reuters) (Spearman's ρ = 0.03, p > 0.9). strategy, or that literature searches typically use the term polyandry over promiscuity.

Conclusions
Arguments over definitions can be tedious, but a cavalier use of borrowed words is unhelpful. Our surveys reveal a tendency to describe female rather than male mating strategies as promiscuous, despite the inherent contradiction in meaning. There was no evidence that journals of different standing publish more or fewer papers that use the term promiscuous, but authors searching for papers using the term promiscuous will generally retrieve lower impact publications.
Promiscuity has become so firmly entrenched in the literature as a synonym for polyandry that its accuracy is no longer questioned. But indiscriminately describing multiple-mating strategies as promiscuous conceals critical features of intriguing evolutionary significance. Indeed, records of truly promiscuous mating strategies, in which females (or males) mated indiscriminately would be remarkable, and predicted, for example, when the costs of mate choice are exorbitant. Like other emotionally evocative terms used to describe sexual behavior [25], promiscuity can be replaced with polyandry, polygyny and polygynandry, as appropriatedescriptive terms that are silent about the nature of mating, and devoid of sociological, psychological and moralistic connotations. Convention is no justification for imprecision, as our survey revealed: without evidence of indiscriminate mating behaviour, 'promiscuity' in evolutionary biology should be left well alone.