A Thousand Tiny ‘Sexes’ or None?

◤ A Thousand Tiny ‘Sexes’ or None? is made available for Open Access publication by funding from Kingston University.
◤ A Thousand Tiny ‘Sexes’ or None? was originally published in the Mycorrhiza and Extancy edition of Sluice magazine, guest edited by Jack Smurthwaite. The edition looks to nature to ask what can be learnt from naturally occurring politics and ecosystems. Mycorrhiza are precise moments of interaction that make complex natural networks, they are the symbiotic relationships that exist between fungi and plants.

  Stella Sandford  
  London, UK  

 March 2020 

Analogies between non-human nature and human behaviour and societies have generally functioned to reinforce or justify a specific aspect of the status quo. This is often more complex than suggesting that various non-human natural phenomena explain or justify particular socio-historical human phenomena (although it is sometimes that crude – for example Thornhill and Palmer’s notorious ‘rape adaptation hypothesis’). 1

See Lynne Segal’s review in Radical Philosophy 106, March/April 2001 for a feminist critique; see also Jerry A. Coyne and Andrew Barry’s take-down in Nature, 09 March 2000.

The analogy between human and plant sexuality at the basis of Linnaeus’s sexual system of classification is an interesting case. As Patricia Fara has suggested, Linnaeus’s privileging of the ‘male’ organ (the stamen) in the sexual system maps an aspect of human society (the dominant position of men) onto the plant world, the seeming ‘naturalness’ of male privilege justifying the ‘naturalness’ of his (in fact arbitrary) decision to privilege the stamen. But, in turn, the door is then open for the apparently ‘natural’ sexual hierarchy in nature to justify male supremacy, which ‘conveniently forgets how this sexual ordering was inferred from society in the first place.’ 2

Patricia Fara, Sex, Botany and Empire: The Story of Carl Linnaeus and Joseph Banks, Icon Books, Duxfird, Cambridge, 2003: 22.

Linnaeus’s ornate descriptions of plant fertilization carry the analogy between human and plant very far, discovering not only analogous sexual organs but parts of the plant (the petals) analogous to ‘bedchamber’ and ‘curtain’ and parts of the process analogous to imagined (gender-stereotypical) human ‘nuptials’. But received wisdom in the history of botany understands the late-eighteenth-century discovery and scientific acceptance of sexuality in plants as a move from a mere analogy between human and plant to the literal ascription of sex to plants. In subsequent years not only plants but also algae, fungi and bacteria would also be sexed according to the same model. But what does this really entail?

This question is complicated by the ambiguity of the word ‘sex’, which is very commonly used both as the generic category encompassing the two types ‘male’ and ‘female’ and for each of those types (‘the sexes), and as shorthand for ‘sexual reproduction’ and sexual intercourse. Lynn Margulis and Dorian Sagan have argued that, for obvious reasons, we have tended to take the large vertebrate mammals (like ourselves) as models when thinking about sex, which leads to the conflation of sex and sexual reproduction, even though ‘mammalian sex is a very late and special variation on a far more general theme’. According to Margulis and Sagan, sex in general is ‘a process characteristic of live organisms only: the complex set of phenomena that produces a genetically new individual, an individual that contains genes (genetic material, DNA) from more than a single source.’ 3

Lynn Margulis and Dorian Sagan, Origins of Sex: Three Billion Years of Genetic Recombination, Yale University Press, New Haven and London, 1986, 2, 9.

This genetic recombination may produce one or more additional individuals (sexual reproduction) but more often the genetically new individual is one of the organisms involved in the sexual process; on the other hand, most reproduction is not sexual (but mitotic). Bacterial sex occurs when two bacteria meet (their outer membranes touching physically) and ‘conjugate’, one ‘donating’ a fragment of DNA to the other.

According to Margulis and Sagan: ‘The fact that we are descendants of that minority of organisms that is sexually reproducing has led us to a very unbalanced and unrealistic view of biological sexuality.’ 4

Ibid., 15.

But as well as the conflation of ‘sex’ and ‘reproduction’, the large vertebrate model also supplies us with a dimorphic and reductive conception of sex in its other sense – two individual ‘sexes’. In biology ‘sexuality’ means the presence of sexual distinction and sexual reproduction, not sexual preference or modes of sexual desire. When sexuality is extended to plants, algae, fungi and bacteria the basic male/female binary of the large vertebrate model is also carried over. In humans and other large vertebrates the male/female distinction is presumed to be distributed across different and in some sense ‘opposite’ individuals, such that ‘male’ and ‘female’ effectively mean ‘male individual’ and ‘female individual’. This popular, vernacular idea of sex is perhaps akin to the enduring ‘folk-biological’ groupings of natural organisms that may well be at odds with formal biological taxonomy (although ‘sex’ is not a formal taxonomical category in any sense). For example, even though biological taxonomy does not recognise ‘tree’, ‘worm’ or ‘bug’ as groups we continue to use these categories meaningfully in everyday life.

Extending ‘sex’ to plants requires us to recognise the vast majority of them as hermaphroditic or ‘monoecious’ – having both male and female parts in the same individual. It seems, then, that the very idea of ‘male’ and ‘female’ begins to move away from the large vertebrate model and folk-biological assumption to name parts or functions, not individuals. Scientific definitions of ‘sex’ then become remote from the everyday (probably primarily morphological) understanding of the division of male and female. In Margulis and Sagan, for example, the definitions rely on an understanding of anisogamy (where mating types have gametes of different sizes): ‘the smaller of a pair of gametes is dubbed “male”. Male sex cells are so designated, however, not only because of their smaller size but because of their propensity to move on their own…. The practical definition of male is simply an organism (gamont) that produces moving, relatively small gametes, often in profusion, but the word may also be used for one of those gametes (or microgametes) itself. The term female, by general definition, usually refers to those gametes which stand still or those gamonts which produce sedentary gametes.’ 5

Ibid., 195.

Anisogamy does not require separate sexes; plenty of anisogamous organisms produce both types of gamete in one individual. This means that this definition of male and female refers primarily to the gametes themselves and only secondarily to gamonts – that is, only secondarily to the organisms carrying the gametes. That it is also apparently possible to distinguish between ‘male’ and ‘female’ unicellular organisms by ‘the presence of a protein on the surface of the undulipodia (as in ciliates) or the existence in one position but not in another of a transposable piece of DNA (as in yeast)’, that is by ‘miniscule molecular differences’, 6

Ibid., 198-9

shores up the sense of the gap between the scientific and the vernacular (folk-biological) understanding of ‘the sexes’.

But could it be that the folk biological idea of ‘the sexes’ also finds its way into biological science? Margulis and Sagan’s work – so radical in other respects – is a stark example that suggests this possibility. Although they decry the anthropomorphism of imagining sex exclusively on the mammalian-human model they remain committed to identifying the different organisms involved in bacterial sex as ‘male’ and ‘female’. In bacterial sex there are ‘donor’ and ‘recipient’ cells. The donor is a bacterial cell possessed of the Fertility factor (F-factor) which enables it to transfer genes to the recipient. Reception of the F-factor turns the recipient into a potential donor (just as donation turns the donor into a potential recipient). Margulis and Sagan call the donor bacterial cell ‘male’ and the recipient ‘female’. But why? Especially when, as bacteria do not have gametes, it conflicts with their own definition of male and female? The fact that they and others call the bacteria involved in non-meiotic recombination ‘parents’ and that bacteria are said to have a ‘sex life’ suggests that the popular language and conceptions of sex and kinship nestle comfortably still at the heart of biology. 7

Ibid., 9, 34, 31.

That the large vertebrate model and its associated heteronormativity misrepresents the biological diversity of sexual forms and behaviour is increasingly recognised. 8

See, for example, Joan Roughgarden, Evolution’s Rainbow: Diversity, Gender, and Sexuality in Nature and People, University of California Press, Berkeley, 2004.

But we may need to dig deeper and develop a suspicion for the very idea of ‘the sexes’. Fungi are the limit case here.

As is now well known, the various fungal strains, which are themselves staggeringly numerous, contain many thousands of different ‘mating types’. Mating types are ‘genetically defined incompatibility groups that at the haploid level [having one set of chromosomes] regulate if successful mating is possible between individuals.’ 9

Bart P.S. Nieuwenhuis and Timothy Y. James, The Frequency of Sex in Fungi, Phil. Trans. R. Soc. B 371: 2016, pp. 2–3.

They are determined by a region of the genome called the Mating Type (or MAT) locus, where the DNA sequence differs within a strain, rendering the types incompatible for mating.

Some fungal species – called ‘bipolar’ – have only two mating types, but some (called ‘tetrapolar’) can have thousands. Neurospora crassa (N. crassa), for example – one of the best-studied fungi – is bipolar, with two morphologically identical ‘mating types’ variously symbolised as ‘A’ and ‘a’ or ‘+’ (plus) and ‘-’ (‘minus’). Initially, the discovery of two mating types (+ and -) in some species was, it seems, understood on the model of two sexes. 10

See A.F. Blakesee, ‘Sexual Reproduction in the Mucorineae’, 1904, Proceedings of the American Academy of Arts and Sciences 40: 205–319: ‘The condition [having + and - types] is essentially similar to that in dioecious plants and animals’. Blakeslee mostly refers to the types as + and -, but also speaks of homothallic forms as ‘bisexual’ and refers to their distinguishing difference as ‘sex qualities’. (213)

But although the difference between mating types here can feasibly be called a ‘sexual difference’ insofar as it is a difference that is determining for sexual reproduction, the two ‘mating types’ are not ‘sexes’. Both mating types are capable of forming the ‘female’ reproductive structure, the protoperithecium, and both produce fertilizing cells which are called ‘male’ by virtue, it seems, of their motility. Of course, we can decide to call the one that in a given instance actually does form the female structure ‘the female’ and thus decide to call the other one the de facto ‘male’. But if we do this, bearing in mind that next time the female might be a male and vice versa, what does this mean for our general understanding of what it means to ‘be’ male or female?

Tetrapolar fungi complicate matters even further. According to Fraser and Heitman: ‘Fungi with a tetrapolar system […] arrange their mating type information in two distinct unlinked regions of the genome, commonly known as the a and b loci. Both of these regions must differ for mating to occur. In many tetrapolar fungi, the mating-type loci are multiallelic [i.e. have multiple gene variants], giving rise to thousands of mating-types in the most extreme examples.’ 11

James A. Fraser and Joseph Heitman, ‘Fungal Mating-Type Loci’, Current Biology, Vol. 13, No. 20, 2003.

As above, these mating type differences can be understood as ‘sexual differences’ – multiple sexual differences – without being different sexes. Once compatible mating types have begun to conjugate, we can decide to say that one has become ‘the male’ and the other ‘the female’ – that is, we can decide to call them ‘sexes’ – but it begins to look like this a habit born of the large vertebrate prejudice, rather than a characterisation of a determining difference between two fungal organisms.

Despite the clear difference between the concepts of ‘mating type’ and ‘sexes’ the scientific literature often still equates them. 12

See, for example, the Preface to Joseph Heitman, James W. Kronstad, John W. Taylor and Lorna A. Casselton, eds., Sex In Fungi: Molecular Determination and Evolutionary Implications, ASM Press, Washington DC, 2007, xv: ‘How could it be that model mushroom species possessed literally thousands of mating types, or sexes, rather than the more pedestrian two sexes common in plants and animals and even many other fungi?’

This is sometimes a celebratory gesture, and to the extent that it contests the binary, large vertebrate prejudice it is welcome.

Here is a rare instance of intellectual convergence in two otherwise very distinct disciplines: continental philosophy and biology. Gilles Deleuze and Félix Guattari’s ‘rhizomatic’ thinking (which encompasses mycorrhiza), leading to the idea of ‘n molecular sexes’ or ‘a thousand tiny sexes’, has proved attractive to feminist theorists contesting the exclusivity of male-female binarism; 13

Gilles Deleuze and Félix Guattari, A Thousand Plateaux, trans. Brian Massumi, Continuum, London/NY, 1987, 275–9; Anti-Oedipus, trans. Robert Hurley, Mark Seem and Helen R. Lane, Continuum, London, 1984. See Elizabeth Grosz, ‘A Thousand Tiny Sexes: Feminism and Rhizomatics’, in Constantin V. Boundas and Dorothea Olkowski, eds., Gilles Deleuze and the Theater of Philosophy, Routledge, NY/London, 1994.

this seems to be literalized in the mycologists’ idea of ‘sexes by the thousands’. 14

See Erika Kothe, ‘Tetrapolar Mating Types: Sexes by the Thousands’, FEMS Microbiology Reviews 19 (1996), 65–87. Kother explains that her title pays homage to J.R. Raper, who wanted to call his 1966 book (published as Genetics of Sexuality in Higher Fungi) Sexes by the Thousands; but 1966 wasn’t ready for this title.

But is there not a more radical lesson from the fungi? Feminist theorists have already suggested that it is time to ditch the large vertebrate prejudice or other variants of it. As Sharon Kinsman says: ‘Shouldn’t a fish whose gonads can be first male, then female, help us determine what constitutes “male” and “female”?’ 15

Sharon Kinsman, ‘Life, Sex, and Cells’, in Maralee Mayberry, Banu Subramaniam and Lisa H. Weasel, eds, Feminist Science Studies, Routledge, New York/London, 2001: 197.

In the same vein, shouldn’t the fungi, whose modes of reproduction relegate the idea of ‘the sexes’ to the background, or disassociate the idea of male and female functions from the idea of individual ‘sexes’, help us to see that ‘the sexes’ cannot be universally presumed as the alpha and omega of sexuality? Who knows what that might mean for us large vertebrates?