Ecology Letters, which I thought was a reasonably respectable journal, has now accepted a “viewpoint” article arguing that there is no consensus on biological sex, and that a definition based on gamete size—a consensus if ever there was one—is just viable as “multivariate” definition that incorporates a combination of chromosomes, genetics, and morphology.
They’re wrong and misguided in many ways, but, as Colin Wright notes in a tweet at bottom, there are so many mistakes and misconceptions in this paper that it would take a full reply to the journal to correct them. I’ll just tender a few comments here, but you can read the paper for free by clicking the title below, or download the pdf at this site.
The authors give three definitions of sex: the classical one based on gamete size (males have small, mobile gametes, females large and immobile ones); a “multivariate” one, popular in some nescient quarters, that defines sex base on some combination of morphology, chromosomes, and “genetics,” and, finally something called “sex eliminativism,” which “eliminates the concept of sex altogether.” They graciously admit that they won’t discuss the last one because “rigorous research on sex-based variation remains vital.” True enough.
But they add that the “rigorous research” they propose be done “also challenges simplistic and harmful ideologies of the sex binary”. This is a red flag that their criticism of the sex binary is partly (if not wholly) based not on biology but on ideology, for the “sex binary” is described as “ideological” and “harmful”. (They are talking, of course, about how a binary may harm people who don’t see themselves as fitting into it.) They later add that there are “ethical and political implications of defining sex.” Only if they care to draw them; most real biologists don’t.
But sex was defined by gamete type long before the “gender” ideology began questioning the view that there are two sexes. And definition has been widely adopted, as I’ve said, not on ideology but on universality and utility. (See this discussion by Richard Dawkins.) All animals and vascular plants have only two sexes corresponding to gamete size, so the gametic definition holds across the animal kingdom. That leads to research questions about why this is so: why do animals, for instance, have only two sexes (some rare parthenogenetic species have only one sex: egg-producing females), but not three or more sexes. There are many papers discussing this question, and the answer seems to be that isogamous species evolve by natural selection to be anisogamous ones (two types of gametes), with that state now seen to be an evolutionarily stable to invasion by more sexes. This already shows that defining sex based on gametes is universal among animals and plants and, because it leads to research questions, also utilitarian. It becomes even more utilitarian when we see that the gametic sex dimorphism helps us understand many facts about biology, most notably the morphological and behavioral differences between males and females explained by sexual selection—an approach first suggested by Darwin in 1871.
What are the problems with a biological sex definition? The authors claim that in most cases biologists don’t look at gametes when discussing or enumerating sexes, and that is usually true. When I divided fruit flies into piles of males vs. females, I looked not at their gametes, but their genitals. This is not a problem because in virtually all species there are proxies for gametes: traits like chromosomes or morphology that are closely correlated with sex. They are not 100% correlated, but pretty close to it.
But that’s not a problem, for the authors don’t seem to realize that there’s a difference between defining sex and recognizing sex. The binary gamete-based definition is universal (and of course useful), while a definitions based on chromosomes, appearance, or genetics is not universal. (Many species have sex determined not by chromosome type or genetics but by rearing temperature, social milieu, haploidy, so on.) Still no matter how sex is determined, if you look at gamete types you always find two sexes. Further, the authors don’t tell us how one is to combine the other traits in a multivariate way to define sex in any species. Would they care to give us a multivariate definition of sex for humans (or any other animal)? They refrain—and for good reason: it would be a futile task.
Their other criticisms of gametic sex are that it doesn’t deal with those species like algae or fungi that don’t have morphologically distinct gametes but are isogamous, with gametes looking the same. These species can have dozens of “mating types” based on genes, each of which can fuse only with gametes of a different type. These have long been called “mating types” and not “sexes” by biologists, and are not a problem for most species we’re interested in—including, of course, humans. As Colin notes below:
But anisogamy (reproduction via the fusion of gametes of different sizes) isn’t meant to apply to isogamous organisms (organisms that reproduce via the fusion of same-sized gametes). Anisogamy and the sexes—male and female—are fully intertwined and inseparable. Isogamous organisms don’t have sexes; they have “mating types.” They’re different from sexes, and that’s why biologists aren’t “inclusive” of isogamous organisms when talking about males and females.
The other criticism of gametic sex are just dumb: we can’t tell the sex of an individual before it produces gametes (like young men [in humans, newborn girls already have eggs!]) or after reproduction has stopped and gametes are no longer produced. From the paper:
. . . this narrow [gametic] definition is not inclusive of reproductive approaches beyond anisogamy (e.g., isogamy) and does not classify organisms before sexual maturity or after reproductive cessation as having a sex.
According to these authors, then, newborn boys do not have a sex (newborn girls do) nor do postmenopausal women or some old men who don’t produce sperm. That is crazy because the gametic definition of sex involves having the biological apparatus to produce large or small gametes; it does not have to be operational. To quote Colin again:
And the notion that a gamete-based definition doesn’t apply to sexually immature individuals or individuals who have ceased producing gametes ignores that the sexes are defined by having the biological FUNCTION to produce small or large gametes—and things still have a function even when it’s not being currently realized.
Below is a table from the paper comparing the gametic versus “multivariate” definitions of sex (the latter broken down into chromosomes, genetics, and morphology), seeing how useful each of the types is in defining sex in nine species (click to enlarge). Note that only one species, the New Mexico whiptail lizard (Aspidoscelis neomexicanus) is said to defy definition by gametes. Yet it is called, in the footnoes, a “female only species”. It is parthenogenetic, formed by the hybridization of two regular species having two gametic sexes, and the hybrids cannot produce males but produce females from unfertilized eggs that are diploid and genetic clones of the mother. So if it’s hard to define organisms in this species as male or female, why do the authors call it a “FEMALE ONLY SPECIES.” Because it produces eggs, Jake! It does not defy the binary at all, and you can put a “yes” in the first column where there’s a “no”.
Note that no other form of classification has “yes” all the way down: not chromosomal definitions, not genetic definitions, not morphological definitions (they again make the ludicrous claim that immature individuals don’t have sexes). And when you combine each of the three univariate non-gametic definitions in some multivariate way, you get a mess. Only the first column, the operational definition using gametes, holds in all organisms. But we already knew that.
There’s another table that’s even more ludicrous. This one points out (as they do in the text, so the table is superfluous) that in some species of hummingbirds, some (not all) females have male-like coloration, even though they have large gametes. There is thus a disparity between the gametic definition of sex and a morphological one. But note that the morphology is used as a species-recognition trait here, not as a way to define sexes. This is one case where a proxy trait for sex doesn’t jibe with the gametes.
Are the females with male-like coloration really males? No biologist would say that, and if you look at the references for the table, you see papers like this (my bolding):
Bleiweiss, R. 1992. “Widespread Polychromatism in Female Sunangel Hummingbirds (Heliangelus: Trochilidae).” Biological Journal of the Linnean Society of London 45: 291–314.
Diamant, E. S., J. J. Falk, and D. R. Rubenstein. 2021. “Male-Like Female Morphs in Hummingbirds: The Evolution of a Widespread Sex-Limited Plumage Polymorphism.” Proceedings of the Royal Society B: Biological Sciences 288: 20203004.
Falk, J. J., D. R. Rubenstein, A. Rico-Guevara, and M. S. Webster. 2022. “Intersexual Social Dominance Mimicry Drives Female Hummingbird Polymorphism.” Proceedings of the Royal Society B: Biological Sciences 289: 20220332.
Falk, J. J., M. S. Webster, and D. R. Rubenstein. 2021. “Male-Like Ornamentation in Female Hummingbirds Results From Social Harassment Rather Than Sexual Selection.” Current Biology 31: 4381–4387.e6.
These all say that the male-appearing hummers are females that have evolved a male-like coloration (they apparently have done to avoid harassment and get more food). These are cases of polymorphism: some of the females look like males, while others look like regular females. The important question is this: why do all the authors call these male-looking birds “females”? It’s not hard to see: they produce large gametes and lay eggs (the authors used other traits associated with female-ness, like body shape in non-mimetic females, to suss out the male-like females). The females that look like males also show territorial behavior characteristic of males, and that’s because biological males have to acquire territories to attract females. Why do only the males do this? Because of the disparity in gamete size—the male mating strategy is to mate with as many females as they can, while females are more selective. (This is a classic behavioral difference due to sexual selection.)
In sum. the authors only buttress the gamete-based definition of sex in their tables. They do show argue that, in cases where you can be deceived about gametes by other traits, biologists like ones studying hummingbirds should describe the criteria they use for assessing sex. That seems okay to me and in fact that’s what’s done in the paper. But sure enough, the authors use color as a proxy for gamete size, not the other way around! Gamete size is fundamental. This is one case, where, as Colin says:
. . . every non-gametic view of sex is logically incoherent and self-refuting because they all rely on gametes as the conceptual anchor.
Here the color serves as a clue to what the conceptual anchor is and, sure enough, it’s gamete size.
In the end, this paper is deeply misguided and, I suspect, driven by ideology rather than biology. What else but ideology would cause four biologists to make such incoherent and misleading arguments? I could think of other reasons, but ideology is the most parsimonious (and the most au courant) given that the authors call the sex binary a “simplistic and harmful ideology” (it’s not an ideology, but an observation) as well as claiming that the definition of sex has ethical and political implications. No, it doesn’t—unless you are an ideologue.
Colin says in his tweet below, “I have reached out to the editors of Ecology Letters asking if they would consider publishing a counter-Viewpoint.” I hope they do. If they don’t, then they are suppressing valid scientific dissent in the name of maintaining a “progressive” ideology. I would like to think that Ecology Letters would do that. Stay tuned.
Here’s Colin’s tweet, which should be expanded to see his take:
🚨ALERT: Top-ranking ecology journal Ecology Letters has published a “Viewpoint” paper titled “There is No Consensus on Biological Sex.”
h/t: Michael
