Eat Prey Love
I wrote the following for a conservation biology class fifteen years ago, when I was but a wee lad. Despite the outdated references, and a few nip-and-tuck edits, I think it’s aged gracefully. I’ve added two updates for some context.
Vero Wynne-Edwards proposed animal species—specifically the red grouse he studied—regulate their own numbers to avoid overexploitation of their food supply. The contention effectively launched modern evolutionary theory, if only in virulent opposition.
George Williams wrote a scathing critique of such theories of group selection. William Hamilton derived the concept of inclusive fitness, whereby relatives help each other to promote their shared genetics. John Maynard Smith, among others, developed an evolutionary game theory, in which altruism was instead a selfish act, part and parcel of a larger tournament of favors and punishments.
The rejoinders amassed into three arguments. Group selection is unlikely because 1) individuals’ rates of birth and death are much greater than those for groups, 2) groups with altruistic members are likely to be invaded by selfish cheaters, and 3) all of Wynne-Edwards’s supposed group selection phenomena can be explained by mechanisms of individual selection.
Two classes of models for group selection managed to survive, even prosper through, this vitriolic assault. Type 1 models of neo-group selection, to be discussed here, found differential group production upon the reproduction rates of individual members. Michael Wade and David Sloan Wilson developed Type 1 models showing a subset of individuals within a population could have comparatively lower fitnesses than their cohorts and still prosper if attributes allowing their group to outcompete —and defend against—cheaters evolved. Ecological structure shields groups from individual selection’s acid efficiency.
These context-specific neo-group selection models have elbowed their way into the respectable literature, leaving Wynne-Edwards and his red grouse in an unmarked grave.
A few sticking points, however, have challenged the orthodoxy even these models share that individual selection is always an efficient regime by which good character designs are produced. Current work on pathogens suggests more benign strains of a virus can outcompete their virulent counterparts within a metapopulation of host bodies. Those virus that reproduce too fast, killing their hosts before transmitting to the next host, epidemiologically burn out. In a fundamental twist to Type 1 modeling, a successful pathogen genotype might cap immediate individual fitness in return for fitness at a different level of organization, with individual-level dividends.
JBS Haldane describes a related cost of natural selection, but directs it within populations. If a mutation arises and frustrates other individuals in the population to zero fitness—no offspring—then the population is likely to go extinct because the mutant itself would be unable to find a mate and small populations tend to go extinct.
It follows that the populations that persist may do so because individual members have characteristics that do not permit exceeding some previous demographic ceiling under which selection took place. As selection requires a certain mortality above and beyond the background death rate, there is an upper bound on the allowable rate—and kind—of character change. The additional mortality can wreck the demographic environment in which reproductive success depends.
It therefore follows that some successful populations may if only by chance refrain from developing genotypes which apportion too high a demographic cost. It might prove detrimental even to individuals with the functionally superior genotype. As survival is an integral part of fitness, that forbearance, to raise Wynne-Edwards from the dead, may extend to genotypes that radically threaten food supplies.
These inbuilt inefficiencies need not be embodied by developmental error, nor caused by limitations imposed by the genetic architecture, including antagonistic pleiotropy. Nor need they be genotypes stuck on a small local hill on an adaptive landscape.
The inefficiencies may instead persist as the aftermath of a failure in a genotypic trajectory. These would be failures caused, for instance, by the inability of one party in a dance of predator-prey coevolution to keep up with the demographic choreography. Many a predator population has eaten itself into extirpation. Prey have also suffered. A suddenly fragmented forest supports few large predators. As a result some prey populations explode only to collapse. On the other hand, those populations that don’t eat themselves out of ecological house and hearth live on.
Environmental resources are as much part of organismal inheritance as the genome. Destroy the landscape, eat prey to oblivion, and organisms ruin their offspring’s prospects.
UPDATE 1. In an effort to resolve a parallax gap between classical niche theory and Stephen Hubbell’s neutral theory of community formation, Andrew Noble and William Fagan more recently derived a nested, stochastic, density-dependent Lotka-Volterra model that concatenates the two approaches. Under a variety of formalisms, the model shows that when intraspecific competition limits population growth, extirpation is delayed longer than expected under neutrality.
No appeal to the Price equation is required. The among-group variation for the genetic component of altruistic behavior need not exceed within-group variation for an ecological ‘altruism’ to arise among non-relations (equation 1 in the graphic). Ecological competition’s mutual frustration—what we might call emergent regulation (equation 2)—can protect a food supply (and over the intermediate run the competitors themselves). As suggested in the post, it’s a natural follow-up to ask whether such demographic inefficiencies might be canalized sensu Waddington into heritable phenotypic checks.
UPDATE 2. Given the inevitable leaps in ideological application, Noble-Fagen serves as no biological rationale for government deregulation and letting the market converge on benevolent gridlock. On the contrary. Capitalist competition, very different from population biology, routinely falls off quasi-equilibria to monopolistic power, or, in the other direction, systemic collapse, the costs of which are routinely externalized.
Consciousness offers us the capacity to impose system boundaries: no one person or class (or company) need sequester so much of what are in fact socially derived resources as to drive the rest of the population to metaphoric or literal starvation, be that for any particular industrial sector or the most vulnerable humanity. That is, we can choose a different fate (including scotching such a frangible system for good).
Much of the passion around the group selection debate grows out of the political economy in which the concept is submerged. So much is at stake. At the center of the Victorian program around which civilization presently orbits are the notions unchecked compound economic growth is a biological imperative and this particular era’s inequality is an ontological constant. The conservation instinct, however, is, contrary to any such kleptocratic metaphysics, as much a part of Earth’s biology as the meat on our bones.
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