Evolutionary theory often suggests competition favors a single, optimal reproductive strategy, leading to the dominance of one male type. The existence of populations where three distinct male forms stably coexist presents a fascinating puzzle for evolutionary biology. This phenomenon, known as polymorphism, describes the occurrence of multiple discrete phenotypes within the same species. When applied to male reproductive roles, it highlights how different strategies can achieve comparable long-term success.
Defining Alternative Male Strategies (AMS)
The coexistence of three different male types is a manifestation of Alternative Male Strategies (AMS). These are heritable, distinct sets of traits that dictate how a male attempts to secure mates and reproductive opportunities. The differences between these morphs extend across morphology, behavior, and even physiology. For instance, one type may be large and highly aggressive, dedicating its resources to defending a large territory and multiple females.
A second type might be smaller, focusing its energy on mate-guarding a single female or territory, utilizing vigilance over brute force. The third type often employs a non-confrontational or “sneaker” tactic, forgoing territory defense entirely in favor of opportunism. Each strategy is an evolutionary package, where the suite of traits—such as body size, hormonal profile, and color display—is finely tuned to maximize reproductive output under specific conditions. Each AMS carries a unique set of trade-offs regarding energy expenditure, risk of injury, and reproductive success.
The Stabilizing Force: Frequency-Dependent Selection
The long-term stability of three male types within a population is maintained by negative frequency-dependent selection (NFDS). This principle describes a scenario where the fitness of a particular strategy decreases as it becomes more common, and conversely, its fitness increases as it becomes rare. If one male type begins to dominate the population, the advantage it enjoys diminishes because the other strategies are specifically adapted to exploit the weaknesses inherent in the common type. This creates a powerful selective pressure that continuously favors the less common types, preventing any one morph from driving the others to extinction.
This dynamic often results in a “Rock-Paper-Scissors” cycle of dominance among the three male types. In this system, Strategy A can defeat Strategy B, Strategy B can defeat Strategy C, but crucially, Strategy C is able to defeat Strategy A. The cycle ensures that the morph frequencies constantly oscillate, but never stabilize at a point where only one type remains. As a morph becomes numerous, it creates an environment where its predator-in-competition thrives, thus reducing the fitness of the abundant morph.
The competitive success of a male is not fixed but is instead dependent on the composition of the local male population it is interacting with.
Real-World Illustration of Triple Polymorphism
A classic example of this triple male polymorphism is found in the common Side-Blotched Lizard, Uta stansburiana, where males exhibit three distinct throat colors: orange, blue, and yellow. The orange-throated males are highly aggressive, ultra-dominant, and defend large territories that encompass multiple females.
The blue-throated males adopt a less aggressive, monogamous strategy, defending a smaller territory and carefully guarding a single female. These mate-guarding blue males are successfully usurped by the aggressive orange males, who are large enough to overwhelm the blue males’ defenses. However, the blue males are highly effective at defending their small territories against the third type of male, the yellow-throated morph.
The yellow-throated males are non-territorial “sneakers” that often mimic the appearance of females, which allows them to bypass the territorial defenses of the dominant males. These yellow males are particularly successful at infiltrating the large, undefended harems of the orange-throated males, mating with females while the orange male is preoccupied with patrolling his expansive boundary. This creates the full cyclical dynamic: the orange morph beats the blue, the blue morph beats the yellow, and the yellow morph beats the orange, ensuring the three strategies remain in perpetual balance.
The Genetic Architecture of Male Morph Evolution
Maintaining these complex, multi-trait strategies requires a specialized inheritance mechanism to prevent beneficial trait combinations from being broken up. This mechanism is the Supergene, a cluster of tightly linked genes that are inherited together as a single unit. The genes within a supergene control the entire suite of traits that define a male morph, including color, body size, and behavior.
The tight linkage within the supergene, often secured by a chromosomal rearrangement like an inversion, drastically reduces the chance of recombination between the genes. This ensures that the successful combination of traits defining a specific strategy—for example, the yellow color, female-mimic behavior, and small body size—is passed down intact from father to son. Without the supergene, recombination would frequently produce intermediate, less-fit morphs, quickly destabilizing the three-way system.