Look away, hunks; this one may sting a bit.

In the wild, the law is straightforward: it’s all about survival of the fittest. But what exactly does fitness mean?

Fitness simply put, is the ability of an organism to successfully leave behind genetic copies, or kids (if you’re mushy). Logic dictates that when we measure metrics like fitness, hunky males end up siring more progeny than meek males — yet this isn’t always the case.

Not every male in the wild is a stud, and yet they still manage to mate. Truly, if only big and burly males breed every season, animal societies would consist mostly of dominant individuals, aside from a few random mutations. However, in reality, they aren’t structured like that.

Generally, there are more meek males than dominant ones. So, how do these meek males not only survive but also manage to reproduce? Often, the answer lies in their sneakiness.

What is sneaky mating? 

Genetic copies are the currency of natural selection. In the game of life, the only goal is to pass on your genetic material—DNA, in the case of multicellular animals—to the next generation. For non-hunky, or ‘sneaky,’ males, the priority is simple: mate, without relying on showmanship or flamboyance. To do this, they had to adopt alternative mating strategies.

Who are the sneaky males? 

Sneaky males aren’t necessarily weak. They might just be younger—less dominant than older males in their prime. Males across taxa have developed strange yet effective alternative strategies to avoid missing out on a breeding season. From gym-bro elephant seals to klepto fish, sneakiness has many faces across the animal kingdom.

Southern Elephant Seals

It’s hard to imagine a 20-foot-long, 5,000-pound (2,268 kg) mammal as anything but dominant, yet not all elephant seals are top dogs. Each year, these seals gather in enormous numbers on rocky beaches to mate. Here, both space and mates are limited. To guard these resources, dominant males, or beachmasters, round up several hundred females and protect their harems to ensure they seal — pun intended — the deal.

In such polygynous setups (one male, multiple females), subordinate or younger males often sneak in to copulate with females while they leave the harems to forage. Away from the ever-vigilant eyes of the beachmasters, young males shoot their shot and ensure their genes make it into the next generation.

Interestingly, it isn’t just males who skirt the beachmasters.

Beachmasters aren’t always the best lovers. In the heat of the moment, females can be injured, gored, or even killed. To avoid such dangers, younger females have been observed skipping traditional breeding sites altogether, opting to pair with younger males at sea rather than risk encounters with beachmasters and their taskmaster tendencies.

“The females have a real choice here. They’re employing a totally non-polygynous alternative mating strategy, which significantly enriches our understanding of polygyny in mammals and other vertebrates,” explained Dr. de Nico de Bruyn, an ecologist studying elephant seals at the University of Pretoria, in an interview with Science.

Blue-gilled Sunfish

Male bluegills have a hierarchy of studs during breeding season. At the top are parentals — big boys who reach sexual maturity at around seven years and build nests to attract mates. Parentals are the only sunfish that make nests. Keep this bit in mind.

Next in line are the sneakers, or cuckolds—small, precocious males that mature early, at the ripe young age of two. Their strategy? Ambush parentals in their nest — mid-spawn, mind you — sneaking in a few sperm while the female sunfish dips to lay eggs.

The final rung in the sunfish hierarchy belongs to the satellites. They have a different approach than both parentals and cuckolds—they don’t hoard females, nor do they sneak sperm.

Instead, these five-year-old males mimic female sunfish to slip into parental nests. Parentals—typically aggressive and inhospitable to cuckolds—are surprisingly tolerant of satellites, mistakenly believing they have two females in the nest rather than one sneaky male hitting on their mate.

The most interesting aspect of sunfish mating isn’t the hierarchy itself; it’s the efficiency. Males like cuckolds and satellites have an astonishingly high fertilization rate. In fact, sunfish females seem to prefer the company of cuckolds, releasing three times as many eggs when mating with them!

Basically, if you’re a male sunfish, ditch the nest. It might not be worth the effort.

Giant Cuttlefish

Most male cuttlefish just want cuddles. Or rather, they want sex. Cuttlefish have short lifespans of one to two years, and of those 24 months, breeding occupies about four months. Essentially, if you’re a cuttlefish, almost a third of your life is spent in an intense search for and competition over sex.

Competition for females leaves a sour taste in the mouths of males across the animal kingdom. Come the breeding season, cuttlefish populations tend to be male-heavy; breeding males always outnumber breeding females. Thus, competition is intense.

To maximize mating probability, males flash their flamboyance to both males and females alike. Sneaky males display one side of their hunky bodies to breeding females while simultaneously channeling their inner woman to present the other side as female to competing males in the region. For context, cuttlefish have the incredible ability to manipulate and change their body color. Nifty, no?

Cichlids

Similar to bluegills, cichlids also engage in gender mimicry. Like satellites in bluegill hierarchy, young or meek male cichlids disguise themselves as females to infiltrate the nests of dominant males. These sneaky males, much like their bluegill counterparts, linger around the nests, waiting for the chance to intercept a prospective female.

Although sneaky mating is common across the Animal kingdom it’s surprisingly limited in fishes. Of the 34,000 or so species of fish in the world, only a dozen engage in such behavior. This makes hierarchies such as those found in cichlids and bluegills all the more special.

Ron Oldfield, a senior biology instructor at Case Western Reserve University, recorded video of a a rare cichlid, the Cuatro Ciénegas, initiating sneaky mating behavior in an ex-situ setup.

Oldfield was able to record this behavior—one of the only instances of sneaky behavior documented across all animals at the time—in a tank in his home office!

Based on his observations, Oldfield stated in a press release that he was able to notice distinct behaviors by the meek male cichlid.

“A large, macho male—the largest fish in the tank—was mating with the largest female in the tank. Another, smaller male was hovering obliquely in the water, hiding next to a large piece of wood near the water surface, and was pointed straight at the mating pair,” explained Oldfield.

The smaller male’s actions were not haphazard either. There was a method to his madness.

“As the female finished a pass, in a sudden burst, the small male dove to the rock, tilted his underside toward the eggs, and then leisurely swam away and went back to his hiding place,” said Oldfield.

Olive Baboons

What do you do when you’re a lowly male with no prospects for love? Find help, of course. In baboons, the sexual hierarchy is an amusing one. Instead of fighting alpha males and facing defeat alone, subordinate males form bromance coalitions, ensuring that at least one of the pair manages to plant their seed for the season. The tactic is simple: one male annoys while the other copulates.

Coalitions aren’t shy with their tactics either; the provoking male doesn’t hold back. In an article published on ScienceLine, Lisa Danish—a researcher at Rutgers University—explained that subordinate male olive baboons often grind their teeth, grunt, and even lunge at the alpha. The bros’ modus operandi is straightforward: they stalk the alpha male and his chosen mate. One member of the pair harasses the alpha, agitating him with aggression while the other hastily mates with the female.”

“You can hear their teeth making this nail on chalkboard kind of awful sound,” explained Danish to ScienceLine.

This tactic, as ridiculous as it sounds, works surprisingly well. As a matter of fact, a recent study quantified that Alpha baboons end up losing the female as much as two out of three times!

Why mate sneakily?

It’s an obvious question: what do animal groups have to lose if only alpha males mate? If these stronger, faster, more appealing individuals are superior to the other males in the group, why shouldn’t they father all the offspring for the generation?

Well, the answer lies in variation. All populations in nature, whether comprised of dominant alleles or not, are vulnerable to being wiped out if they lack heterogeneity. In this sense, sneaky mating acts as a self-regulating factor to ensure that the genetic makeup of groups never stagnates or succumbs to inbreeding pressures. It forces us to rethink current ideas regarding evolutionary fitness. The very existence of sneaky mating behaviors is a testament to their effectiveness, having been tried and tested over many generations; they are valid evolutionarily stable strategies.

Remember survival of the fittest? It’s not always about being the biggest or toughest; the phrase simply means that those who can adapt the most to their circumstances have the best odds of surviving and passing on their genes. Sometimes, it’s the sneaky ones who come out on top. Ultimately, fitness is all about passing on your genes, and sneaky subordinate cuckolds seem to be thriving in that department.