Open Access

Promiscuous words

Frontiers in Zoology201310:66

https://doi.org/10.1186/1742-9994-10-66

Received: 22 October 2013

Accepted: 5 November 2013

Published: 8 November 2013

Abstract

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 19th 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. [36] 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 polyandry – the 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 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. [1618]. 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 mating – whether either sex is discriminating or not – and 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 meta-analyses). 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.
Table 1

Details of papers published in the journal Animal Behaviour that make reference to promiscuity

Title of paper

Publication details ( Animal Behaviour) year, volume, page numbers

Reference to promiscuity

Female choice?1

  

Title

Abstract

Text

Key-words

Sex

 

Models of parent-offspring conflict 2. Promiscuity

1978, 26: 111–122

Yes

Yes

Yes

No

Female

Postcopulatory mate guarding delays promiscuous mating by female decorated crickets

1994, 48:1479–1481

Yes

Yes

No

Female

Yes

Mate sampling in a population of sand gobies

1997, 53: 267–276

No

Yes

Yes

No

Both

Yes

Behavioural correlates of monogamy in the noisy miner, Manorina melanocephala

1997, 54: 571–578

No

Yes

Yes

No

Female

No

Spawning success in the damselfish Amblyglyphidodon leucogaster: the influence of eggs in the nest

1998, 55: 651–664

No

Yes

Yes

No

Both

Yes

Behavioural aspects of the raccoon mating system: determinants of consortship success

1999, 57: 593–601

No

Yes

Yes

No

Female

Yes

Male mating behaviour and sperm production characteristics under varying sperm competition risk in guppies

1999, 58: 1001–1006

No

Yes

Yes

No

Female

Yes

Effects of body size and home range on access to mates and paternity in male bridled nailtail wallabies

1999, 58: 121–130

No

Yes

Yes

No

Both

Yes

Proximate factors associated with high levels of extra-consort fertilization in polygynous grey seals

1999, 58:527–535

No

Yes

Yes

No

Female

Yes

Sexual selection and the evolution of exclusive paternal care in arthropods

2000, 60: 559–567

No

Yes

Yes

No

Male

Lack of parasite-mediated sexual selection in a ladybird/sexually transmitted disease system

2002, 63: 131–141

No

Yes

Yes

No

Both

No

Sexual selection, multiple mating and paternity in grey mouse lemurs, Microcebus murinus

2002, 63: 259–268

No

Yes

Yes

No

Both

Yes

Genetic monogamy in Monteiro's hornbill, Tockus monteiri

2002, 63: 787–793

No

Yes

No

No

Female

No

The effects of sexual selection and life history on the genetic structure of redfronted lemur, Eulemur fulvus rufus, groups

2002, 64: 557–568

No

Yes

Yes

No

Female

No

Effects of repeated mating and polyandry on the fecundity, fertility and maternal behaviour of female earwigs, Euborellia plebeja

2003, 65: 205–214

No

Yes

No

No

Female

No

Spacing behaviour and its implications for the mating system of a precocial small mammal: an almost asocial cavy Cavia magna?

2003, 66: 225–238

No

Yes

Yes

No

Female

No

Behavioural defenses against sexually transmitted diseases in primates

2003, 66: 37–48

No

Yes

Yes

No

Female

Extrapair paternity in the common sandpiper, Actitis hypoleucos, revealed by DNA fingerprinting

2004, 67: 333–342

No

Yes

Yes

No

Female

No

Spacing pattern in a social group of stray cats: effects on male reproductive success

2004, 68: 175–180

No

Yes

Yes

No

 

No

Extrapair paternity and offspring immunocompetence in the reed bunting, Emberiza schoeniclus

2004, 68: 283–289

No

Yes

Yes

No

Female

Yes

Estimates of extreme sperm production: morphological and experimental evidence from reproductively promiscuous fairy-wrens (Malurus)

2004, 68: 541–550

Yes

Yes

Yes

No

Female

Yes

A pair choice test to identify female mating pattern relative to ovulation in longtailed macaques, Macaca fascicularis

2005, 70: 1283–1296

No

Yes

Yes

No

Female

No

Context-dependent male mating preferences for unfamiliar females

2005, 70: 1429–1437

No

Yes

Yes

No

Male

No

Social modulation of androgens in male vertebrates: meta-analyses of the challenge hypothesis

2006, 71: 265–277

No

Yes

Yes

No

Female

Number of mates and timing of mating affect offspring growth in the small marsupial Antechinus agilis

2006, 71: 289–297

No

Yes

Yes

No

Both

Yes

Variation in the cost to females of the sexual conflict over mating in the seed bug, Lygaeus equestris

2006, 72: 313–321

No

Yes

Yes

No

Both

No

The impact of lekking on the spatial variation in payoffs to resource-defending topi bulls, Damaliscus lunatus

2008, 75: 1229–1234

No

Yes

No

No

Female

Yes

Investment in eggs is influenced by male coloration in the ostrich, Struthio camelus

2009, 77: 1027–1032

No

Yes

Yes

No

Both

No

Male coloration reveals different components of immunocompetence in ostriches, Struthio camelus

2009, 77: 1033–1039

No

Yes

Yes

No

Both

Yes

Paternity assurance through frequent copulations in a wild passerine with intense sperm competition

2009, 77: 183–187

No

Yes

No

No

Female

No

Quantifying and comparing mating systems using normalized mutual entropy

2009, 77: 201–206

No

Yes

Yes

Yes

Both

Do male guppies distinguish virgin females from recently mated ones?

2009, 77: 425–431

No

Yes

No

No

Female

Yes

Another genetically promiscuous ‘polygynous’ mammal: mating system variation in Neotoma fuscipes

2009, 77: 449–455

Yes

Yes

Yes

Yes

Both

No

Male dominance rank and reproductive success in chimpanzees, Pan troglodytes schweinfurthii

2009, 77: 873–885

No

Yes

Yes

No

Female

Yes

Male feeding rate and extrapair paternity in the facultatively polygynous spotless starling

2009, 78: 1335–1341

No

Yes

Yes

No

Female

No

Male mate-searching strategies and female cues: how do male guppies find receptive females?

2010, 79: 1191–1197

No

Yes

Yes

No

Female

Yes

Plumage coloration, ejaculate quality and reproductive phenotype in the red-backed fairy-wren

2010, 79: 1239–1246

No

Yes

Yes

No

Female

Yes

Male aggression and sexual coercion in wild West African chimpanzees, Pan troglodytes verus

2010, 79: 333–342

No

Yes

No

No

Both

Yes

Sperm removal, ejaculation and their behavioural interaction in male cuttlefish in response to female mating history

2010, 79: 613–619

No

No

Yes

Yes

Both

No

1Not included for theoretical or review papers.

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 strategy, or that literature searches typically use the term polyandry over promiscuity.
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).

Table 2

Characteristics of papers retrieved by the search term ‘promiscuity’ or ‘promiscuous’ and ‘polyandry’ and ‘polyandrous’ in 13 journals from 2000 to 31st July 2013

Journal

Journal Impact Factor1

Papers retrieved by the search term ‘Promiscuity’ or ‘Promiscuous’

Papers retrieved by the search term ‘Polyandry’ or ‘Polyandrous’

% papers retrieved by promiscuous3

Δ cites4

  

Papers

Most cites in a paper

Mean cites per paper

h-index2

Papers

Most cites in a paper

Mean cites per paper

h-index2

  

American Naturalist

4.55

9

205

43

7

21

118

24

13

30.0

19

Animal Behaviour

3.07

39

118

15

14

79

663

26

22

33.1

−11

Behavioral Ecology

3.22

21

54

14

9

57

67

16

19

26.9

−2

Behavioral Ecology & Sociobiology

2.75

40

50

15

15

81

51

18

23

33.1

−3

Biology Letters

3.35

6

35

10

4

18

29

10

8

25.0

0

Current Biology

9.49

13

37

9

5

14

146

32

7

48.1

−23

Ecology Letters

17.95

2

74

37

1

8

137

32

4

20.0

5

Ethology

1.95

11

37

12

5

30

120

16

12

26.8

−4.5

Evolution

4.86

23

103

23

12

65

113

28

28

26.1

−5

J Evolutionary Biology

3.48

17

62

13

9

58

86

21

22

22.7

−8

Molecular Ecology

6.28

20

90

24

13

62

421

31

27

24.4

−7

Nature

38.6

6

142

57

4

7

261

119

7

46.2

−62

Proc Nat Acad Sci USA

9.74

7

106

35

6

10

128

42

8

41.2

−7

Proc Royal Society B

5.68

37

106

39

24

83

128

32

33

30.8

7

Science

31.03

2

122

48

3

6

148

61

6

25.0

−13

(Note, Frontiers in Zoology is not included in the survey because no papers are retrieved by the search terms promiscuity or promiscuous, and only two papers were retrieved by the search terms polyandry or polyandrous).

12012 Journal Citation Report®, ISI Web of Knowledge™.

2h-index calculated according to J.E. Hirsch in ISI Web of Knowledge™.

3Calculated 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.

4The mean cites per paper retrieved by the search terms promiscuity or promiscuous less the mean cites per paper retrieved by the search terms polyandry or polyandrous.

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 appropriate – descriptive 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.

Declarations

Acknowledgements

We thank Malin Ah-King, Cordelia Fine, Root Gorelick and an anonymous referee for their insights. The Australian Research Council (DP0558265 to MAE and TMJ; DP0987360 to MAE; and DP110101163 to KBM) and the University of Melbourne (Career Interruption Research Fellowship to TMJ) support our research on the mating behavior of animals.

Authors’ Affiliations

(1)
Department of Zoology, University of Melbourne
(2)
Centre for Evolutionary Biology, The University of Western Australia

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Copyright

© Elgar et al.; licensee BioMed Central Ltd. 2013

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

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