How the Perception of an Animal Can Shape the Evolution of a Plant for No Mutual Benefit
By Eben van Tonder, 18 March 25
Referencing The Carrion Flower: An Evolutionary and Cultural Study of Stapelia and The Carrion Flower and the Unanswered Questions of Evolutionary Precision
Introduction: Life Beyond Mutualism
In The Carrion Flower and the Unanswered Questions of Evolutionary Precision, I posed a fundamental question: How did Stapelia, a plant, evolve to so perfectly replicate the appearance, smell, and even texture of rotting flesh? And more importantly, why did this occur in such an exploitative way?
Unlike mutualistic examples—figs and wasps, orchids and bees, or humans and their domesticated crops—this is a relationship that benefits only the plant. The carrion fly, lured by deception, receives nothing. No food. No reproductive opportunity. No gain. The fly’s behaviour is hijacked; its intention—the drive to locate decaying flesh and reproduce—becomes the coordinating principle around which Stapelia’s entire evolutionary strategy revolves.
This is not co-evolution in the traditional sense. It’s one-sided manipulation. And it raises a deeper question: Can the intentional behaviour of an animal, with no benefit to itself, act as a coordinating force in shaping another organism’s evolution?
The Central Thesis: The Fly’s Intention as the Coordinating Principle
What guides the evolution of Stapelia is not the fly’s biology alone, but its intention—its hardwired goal of locating carrion. The plant doesn’t adapt to the fly’s physiology directly; it adapts to the fly’s expectations, its cognitive model of what carrion is.
This is more than sensory exploitation. It’s behavioural exploitation, where the subjective experience of the fly becomes the template the plant must mimic. The fly is not consciously selecting for flowers that look like carrion. But its intention-driven behaviour filters which plants succeed in passing on their genes. In this feedback loop, the fly’s perceptual world becomes the evolutionary shaping force.
Sensory Exploitation and Deception: Theoretical Frameworks and Scholars
Michael J. Ryan: Sensory Exploitation and the Evolution of Deception
Michael J. Ryan’s A Taste for the Beautiful (2018) provides a compelling framework for understanding sensory exploitation in evolution. Ryan’s research focuses primarily on sexual selection and mate choice in animals, particularly frogs and fish, but his principles apply more broadly to how organisms exploit the sensory preferences of others.
Ryan introduces the concept of sensory bias: pre-existing preferences in an organism’s sensory or cognitive system that can be co-opted by another species. In many species, these biases evolved for entirely different purposes—for example, a female fish might be hardwired to be attracted to a particular shape or colour because it indicates food or safety. A male fish that happens to develop an ornament mimicking this signal can hijack the female’s attention, gaining a reproductive advantage.
He calls this sensory exploitation, where one organism evolves traits specifically designed to tap into and manipulate these hardwired biases. Ryan makes it clear that the key to sensory exploitation is understanding the receiver’s sensory world:
“The sender, whether a male bird or an orchid flower, succeeds not because it simply evolves an attractive trait, but because it evolves a trait that fits into the pre-existing perceptual world of the receiver.”
— A Taste for the Beautiful, p. 14.
But Ryan’s examples often involve mutual benefit—or at least, minimal cost to the deceived. In swordtail fish and túngara frogs, both sexes stand to gain from successful mate choice, even if biases are exploited. In the case of Stapelia, however, there is no benefit to the fly. Its sensory bias for carrion—a bias necessary for its reproductive success—is ruthlessly hijacked. The fly lays its eggs on the flower, and its larvae die. Ryan himself acknowledges that sensory exploitation can tip into deception, but rarely explores cases where the cost to the deceived is so high and no adaptive feedback seems to exist to counterbalance it.
This is where Stapelia pushes Ryan’s framework to its extreme. The perceptual world of the fly becomes not just a channel for communication, but a prison in which its behaviour is predictable, reliable, and exploitable, without escape.
Amotz Zahavi: The Handicap Principle and the Problem of Dishonest Signalling
Amotz Zahavi’s Handicap Principle, introduced in 1975 and further elaborated in The Handicap Principle: A Missing Piece of Darwin’s Puzzle (1997), provides an evolutionary explanation for how honest signalling evolves. Zahavi argued that reliable signals must be costly to produce. The classic example is the peacock’s tail: a large, cumbersome, metabolically expensive structure that signals genetic quality precisely because only a healthy male can afford to carry it. Such signals are honest because they cannot be faked without incurring prohibitive costs.
But where does deception fit in? Zahavi acknowledges that cheating and dishonest signalling can and do evolve, particularly when enforcement mechanisms are absent. In many species, individuals can evolve deceptive signals if the receiver cannot easily test or verify the signal’s authenticity.
Zahavi writes:
“The opportunity for cheating arises when the cost to the receiver of being deceived is low enough that it doesn’t evolve resistance.”
— The Handicap Principle, p. 165.
In Stapelia, we see exactly this. The cost to the individual fly of being deceived is high (it loses reproductive success), but the fly population as a whole does not exert enough selective pressure on the plant to evolve resistance. Carrion flies are r-strategists—they produce many offspring and have short lives. The deception isn’t enough to drive a significant evolutionary response. This allows Stapelia to persist in its deception without ever paying the evolutionary “cost” of being detected or ignored.
What Stapelia demonstrates is that the Handicap Principle doesn’t apply universally. Stapelia has evolved dishonest signals—smells, colours, textures—that cost very little but deliver high rewards. And because the fly lacks agency or feedback mechanisms, the deception remains stable over evolutionary time.
Donald R. Prothero: Evolutionary Complexity and the Appearance of Purpose
Donald R. Prothero’s work, especially Evolution: What the Fossils Say and Why It Matters (2017), addresses the illusion of purpose in nature. He emphasizes that natural selection can create structures and behaviours so complex, precise, and effective that they seem designed, even though they are the result of blind evolutionary processes.
Prothero focuses on convergent evolution and mimicry as examples. He points out that organisms like the orchid Ophrys, which mimics female bees to attract male pollinators, demonstrate how random mutations and natural selection can produce deceptive strategies that are highly successful.
But Prothero also acknowledges the limits of our understanding. Some mimicry systems, particularly Batesian mimicry, can evolve rapidly and maintain stability despite imbalanced cost-benefit ratios.
“These systems push the boundaries of what we can comfortably explain through gradualism alone.”
— Evolution, p. 352.
Stapelia represents one of those cases where the precision of the mimicry—down to chemical compounds like putrescine and cadaverine, visual marbling patterns, tactile hairs, and even solar-absorption heating effects—seems to transcend what gradual evolution should readily explain.
Prothero’s framework defends natural selection as a sufficient mechanism but admits that extreme cases challenge our ability to trace exact adaptive pathways. Stapelia may well be such a case.
Chemical Proof of Deception: Putrescine and Cadaverine in Stapelia
Stapelia doesn’t just mimic carrion in appearance; it produces the exact molecules that trigger the fly’s innate behaviours. Putrescine and cadaverine are biogenic amines, responsible for the smell of decaying animal flesh. They are produced by the bacterial breakdown of ornithine and lysine during decomposition. In the animal world, these chemicals signal death and decay, attracting scavengers and insects.
Stapelia produces these same compounds biosynthetically. This isn’t incidental. No other plant is known to produce such high concentrations of these chemicals for pollination deception. In some legumes, small amounts of putrescine and cadaverine exist, usually in defensive pathways or growth regulation, not as attractants (Tiburcio et al., 1997). Stapelia, in contrast, synthesises them specifically to mimic carrion and exploit fly behaviour (Jürgens et al., 2006).
This is not a cooperative interaction. The fly lays eggs on a false substrate, its larvae doomed to starve. The plant benefits, the animal does not.
Implications of the Coordinating Principle: Who Shapes Whom?
At the heart of this mystery lies an unsettling question: Did the fly’s intentional behaviour create the flower’s form? If the fly, through its choices, determined whether one flower reproduced and another did not, its preference became law. The fly’s sensory world effectively moulded the flower’s reality.
This dynamic suggests that the Carrion Flower and its pollinator are engaged in a feedback loop, where the intentions and perceptions of one organism have shaped the body and behaviour of another. And if this is true for Stapelia and the fly, is it not also true for other organisms, including ourselves?
Parallels in Nature? Why Stapelia Is Uniquely Exploitative
In much of biology, we see co-evolutionary relationships where two species shape one another over time—often to mutual benefit. Classic examples include: figs and fig wasps; orchids and pollinator bees; humans and domesticated crops or animals.
But these systems are fundamentally different from the relationship between Stapelia and the carrion fly. In co-evolution, both species gain: figs offer wasps a site to lay eggs, while the wasps pollinate the fig; orchids may deceive male bees briefly, but the interaction provides at least reproductive opportunity; domesticated animals and crops benefit through artificial selection, increasing their populations and reproductive success via human intervention.
In these systems, agency is often shared. Humans intentionally select for traits in crops and animals, often conscious of the benefits to themselves but also ensuring the survival and spread of the organisms they cultivate. The animal or plant benefits—sometimes as a partner, sometimes as a tool—but both are shaped by mutual reinforcement.
What Happens with Stapelia Is Not Mutualism
The carrion fly gains nothing. Its reproductive behaviour is exploited. It invests energy, laying eggs that never develop, on a false promise. The fly’s intention—to find carrion and reproduce—drives its behaviour. That intention becomes the coordinating principle that sculpts Stapelia‘s form. But the fly has no say, and its genetic fitness may even be reduced by the deception.
This is not co-evolution in the classic sense, where two species shape each other symbiotically. It is asymmetrical evolutionary manipulation, though not in the traditional sense of parasitism, because Stapelia doesn’t kill the fly. It tricks it into performing a vital task—pollination—while offering nothing in return.
Why Agriculture Is Not the Same
In human agriculture, we intentionally breed plants and animals. These organisms: reproduce more successfully, expand their ecological reach, and benefit from human stewardship. Even if human intention is self-serving, the domesticated species win, expanding into environments they would never have otherwise occupied.
By contrast, the fly doesn’t benefit from Stapelia. There is no mutual survival, no symbiosis, no spread of the fly due to its interaction with the plant. There is no agency from the fly in shaping Stapelia; it is passive, manipulated solely by its pre-existing perceptual biases.
The Moment of Choice: How Did Stapelia “Choose” the Fly?
This question strikes at the heart of the mystery. Why the fly? Why mimic carrion? Why this particular path, when countless others were possible?
The Beginning of Mimicry: A Hypothetical Pathway
Some early Stapelia ancestors may have produced foul-smelling volatiles as a defence mechanism against herbivores. Small changes in chemical output could have inadvertently attracted carrion flies, who briefly visited the flower, inadvertently transferring pollen.
Any variant that increased fly visits—whether through scent, colour, or texture—would have gained a reproductive advantage. From that point, selection pressure would drive increasing refinement of the mimicry. But the direction was locked in: the fly’s intentionality—its need to locate carrion—became the coordinate axis along which the plant’s evolution proceeded.
The plant did not “choose” in the conscious sense. It was channelled by the perceptual field of its pollinator.
Philosophical Reflections on “Choice” and Direction
Brian Goodwin, in How the Leopard Changed Its Spots (1994), argued that form arises from self-organising systems influenced by environmental inputs. Yet Stapelia’s form seems less like self-organisation and more like organismic negotiation with the fly’s senses. Stuart Kauffman, in The Origins of Order (1993), discusses adjacent possibles in evolution. Stapelia entered a narrow evolutionary corridor once it began exploiting the fly. But the narrowness suggests constraint not just by chance, but by structured feedback from the fly’s perception.
The Coordinating Force of Intention: A New Understanding?
The fly’s intention—its drive to find carrion—became the evolutionary blueprint for Stapelia. This is not conscious coordination, but a functional coordination nonetheless. The fly’s inner world, its perceptual framework, determined the selective landscape.
Implications
Intention shapes form, even when the intending organism does not benefit. Cognitive models—even simple, hardwired ones—can guide evolutionary outcomes. Life may evolve not only through environmental pressures, but through psychological landscapes.
What This Means for Humans
If a fly’s unconscious intention can shape another organism’s evolution, what about us? Humans intentionally shape their world: agriculture, animal domestication, urban ecosystems. But even our unconscious biases, desires, and preferences may be coordinating principles—driving the evolution of pathogens, pests, and even social structures.
Our attention and intention, both conscious and unconscious, create selective environments that shape life.
As Loren Eiseley once wrote,
“The world is not a prison-house, but a kind of spiritual garden. The human mind is not confined within the cranium like a prisoner in a cell, but walks abroad with its senses, and gathers impressions, and turns them into creations.”
(The Night Country, 1971)
Eiseley’s words remind us that our perception and intention are not passive. They create.
Conclusion: The Lesson of the Carrion Flower
Stapelia shows us that life’s complexity arises not just from external conditions, but from internal drives and perceptions. The fly’s intention created a niche Stapelia exploited. We, too, live in a world we partly create—by what we choose to see, pursue, and value.
Perhaps we should be more aware of the unseen power of our intentions. Not because they can change the world. But because they already do.
References
van Tonder, E. (2025). The Carrion Flower and the Unanswered Questions of Evolutionary Precision. Earthworm Express.
van Tonder, E. (2025). The Carrion Flower: An Evolutionary and Cultural Study of Stapelia. Earthworm Express.
Dawkins, R. (1982). The Extended Phenotype. Oxford University Press.
Ryan, M. J. (2018). A Taste for the Beautiful. Princeton University Press.
Zahavi, A., & Zahavi, A. (1997). The Handicap Principle: A Missing Piece of Darwin’s Puzzle. Oxford University Press.
Prothero, D. (2017). Evolution: What the Fossils Say and Why It Matters. Columbia University Press.
Tiburcio, A. F. et al. (1997). Polyamine metabolism and its regulation. Physiologia Plantarum, 100(3), 664-674.
Jürgens, A. et al. (2006). The chemical nature of fetid floral odours in stapeliads and carrion flowers. New Phytologist, 172(3), 452-468.
Goodwin, B. (1994). How the Leopard Changed Its Spots. Charles Scribner’s Sons.
Kauffman, S. A. (1993). The Origins of Order. Oxford University Press.
de Waal, F. (2016). Are We Smart Enough to Know How Smart Animals Are? Norton