The Red Queen, and what actually transfers

There is an image I keep being offered at conferences, and I keep declining. The Red Queen: you have to run as fast as you can just to stay in the same place. It is used to describe modern working life, and it is used as encouragement. Both of those are misreadings, and the second one is worse.

What Van Valen actually said

Leigh Van Valen published “A new evolutionary law” in 1973, in a journal he had founded himself after the paper was rejected elsewhere. Its empirical core is not a metaphor at all. It is the Law of Constant Extinction: from fossil survivorship curves, the probability that a taxonomic group goes extinct in a given interval is roughly constant through time. A lineage that has persisted for fifty million years is no less likely to disappear in the next interval than one that appeared yesterday. Age confers no protection.

The Red Queen is the proposed explanation for that pattern, not the pattern itself. In a zero-sum resource environment, each species’ improvement degrades the environment of everything it interacts with, so continuous adaptation buys no net gain in relative fitness. Alice is an illustration of a deduction from a regression on fossil data.

Which means the popular reading inverts the claim. Van Valen’s point is that running produces no relative gain — a statement about the futility of accumulated advantage in a coevolving system. As motivational material it is close to the opposite of what it says.

Three other things it is not

• It is not the Red Queen hypothesis for sex. The idea that sexual reproduction persists because parasites track common host genotypes is Jaenike, Hamilton and Bell, from 1978 onwards. Van Valen’s 1973 paper was not about sex. When a popular article says “the Red Queen explains why sex evolved”, it is not citing Van Valen.
• It is not an arms race. Fluctuating selection — cycling, no net directional change — and escalation — directional, cumulative — make opposite predictions. They are routinely merged into one image of two species building bigger weapons. They are different phenomena.
• It is not a pairwise story. Van Valen described a constantly changing, coevolving ecological theatre of interconnected networks. Reducing it to predator and prey loses the part that made it a law.

Where it is genuinely demonstrated

Red Queen dynamics are real, and the evidence is beautiful. My favourite is resurrection ecology: Daphnia and their parasite Pasteuria hatched out of dated pond sediment layers and cross-infected across time, with parasites most infective against their contemporary hosts. Time-lagged, cycling coevolution, recovered from mud. More recently, twenty years of tuberculosis-driven selection on meerkat immune genes in a wild population.

Host and pathogen: demonstrated. Host and its own commensal gut bacteria: not. I looked, because I wanted it to be there — it would tie my two research lives together neatly. The established framework for commensals is mutualism, phylosymbiosis and co-diversification, not antagonistic cycling. The bacterial transporter my colleagues and I published in 2023 prevents intestinal inflammation. That is not an arms race. That is a negotiated settlement.

The line I am drawing

So here is the boundary, stated as a boundary rather than hidden in a hedge.

• Measured. Constant extinction probability in the fossil record. Cycling host–parasite coevolution in specific systems. Predictive regulation in physiology — the brain anticipating demand and adjusting in advance, which is what allostasis actually claims and which is well supported.
• Inferred. That chronic occupational stress associates with adverse biology. The effects are real, modest, observational and heavily confounded by socioeconomic position.
• Imagery. The Red Queen applied to your workload. Moving from taxa to individuals, from a million years to a fortnight, from relative fitness in a zero-sum ecosystem to subjective demand, and from coevolution to no mechanism at all. Nothing survives that transfer except the picture.

Why I still use the image

Because it is an excellent picture, and pictures do real work. What it captures accurately is the experience of effort that buys no accumulated advantage — the sense that last year’s adaptation has already been absorbed into this year’s baseline, and that the work of staying functional never converts into a reserve.

That experience is genuine, and naming it helps. What is not legitimate is to call it evolutionary biology and let the borrowed authority do the persuading.

What does transfer

Allostasis transfers, and it is the more useful idea anyway. The claim is that the body does not defend fixed setpoints and correct errors afterwards; it predicts demand and adjusts in advance, trading local constancy for whole-organism efficiency. That genuinely reframes stress: not as damage inflicted from outside, but as a budget allocated in advance, sometimes wrongly.

What allostasis does not give anybody is a number for how much demand a given person can take. Allostatic load is a well-specified concept with a badly standardised measurement — no consensus biomarker set, arbitrary quartile scoring, and heavy overlap with ordinary cardiometabolic risk. It is a measure of accumulated cost, not of remaining capacity, and the two are constantly confused.

Which leaves us with a correct picture of how the body anticipates demand, and no instrument for how much it can take. That is an uncomfortable place to work from. It is also the true one, and I would rather build there than on a metaphor with a citation stapled to it.

• Van Valen L — A new evolutionary law. Evolutionary Theory 1:1–30, 1973. (No DOI: the journal was founded by the author.)
• Solé R — Revisiting Leigh Van Valen’s “A New Evolutionary Law” (1973). Biological Theory 17:120–125, 2022.
• Decaestecker E, et al. — Host–parasite “Red Queen” dynamics archived in pond sediment. Nature 450:870–873, 2007.
• Brockhurst MA, et al. — Running with the Red Queen: the role of biotic conflicts in evolution. Proc R Soc B 281:20141382, 2014.
• Sterling P — Allostasis: a model of predictive regulation. Physiology & Behavior 106:5–15, 2012.
• McEwen BS — Protective and damaging effects of stress mediators. New England Journal of Medicine 338:171–179, 1998.
• Ramsay DS & Woods SC — Clarifying the roles of homeostasis and allostasis in physiological regulation. Psychological Review 121:225–247, 2014.
• Guidi J, et al. — Allostatic load and its impact on health: a systematic review. Psychotherapy and Psychosomatics 90:11–27, 2021.
• Liuu S, Nepelska M, et al. — Identification of a muropeptide precursor transporter from gut microbiota and its role in preventing intestinal inflammation. PNAS 120, 2023.