Wild Neighbors: Los Machos Furtivos

By Joe Eaton
Saturday November 26, 2011 - 09:18:00 AM
Red-sided garter snake: deceptive pheromones.
Zooplan (Wikimedia Commons)
Red-sided garter snake: deceptive pheromones.
Typical male western marsh harrier: not in drag.
Boldings (Wikimedia Commons)
Typical male western marsh harrier: not in drag.

Hot news from Europe: in a population of western marsh harriers (Circus aeruginosus) in France, 40 percent of the males are crossdressers . Typical males of this hawk species, a close relative of our northern harrier, have overall streaky-brown plumage. Females have whitish heads and shoulders, and so do female-mimicking males. Typical males don’t seem to recognize the mimics as rivals. Audrey Sternalski, Francois Mougeot, and Vincent Bretagnolle report in Biology Letters that typical males attack decoys with their own kind of plumage at a higher rate than those with female-mimic plumage. What the mimics get out of it is access to the mates—up to three, depending on available resources—of territory-holding typical males. 

Welcome to the club, Circus aeruginosus. There’s a lot of this kind of thing going on. In animals as disparate as cuttlefish, toadfish, lizards, and sandpipers, some males use their resemblance to females to outcompete other males for mating opportunities. With some, the deception is opportunistic and temporary; for others, a lifelong commitment. They’ve been variously called jacks, she-males, sneakers, streakers, scroungers, satellite males, cuckolders, parasitic spawners, and machos furtivos. 

In his groundbreaking Descent of Man, Charles Darwin identified two evolutionary paths for male reproductive success. One involves size, brute force, and/or weaponry: males that can physically dominate or damage rivals mate with more females and bequeath more of their genes to future generations. That’s the trajectory leading to the bull elephant seal and the silverback gorilla. The other path invokes female preference for good-looking males, selecting for brilliant plumage or elaborate courtship displays as signals of robust health. 

The evolution and persistence of female-mimicking males and other sneaker variations suggests a third way for sexual selection: alternative reproductive strategies that coexist with male reliance on brawn or beauty. To paraphrase Ecclesiastes, the battle is not always to the strong, but the race is sometimes to the swift (and sneaky). 

One creature is able to switch its resemblance to the opposite sex on and off. Giant cuttlefish (Sepia apama), relatives of the octopus and squid, gather in breeding swarms off the coast of South Australia, where large males attempt to monopolize the attentions of females. All cuttlefish can vary their appearance by expanding and contracting specialized skin cells called photophores. According to Mark D. Norman, Julian Finn, and Tom Tregenza, small males assuming typical female patterns and body shapes shadowed mating pairs. If the mate-guarding male was distracted, the interloper resumed a male-distinctive pattern and attempted to mate with the female, often successfully. The authors speculate that this kind of “dynamic sexual mimicry” may have driven the cephalopods’ remarkable ability to change their shapes and colors. 

Red-sided garter snakes (Thamnophis sirtalis parietalis) may be a borderline case. These snakes spend the winter in mass hibernacula in Manitoba. When they emerge in the spring, males seek out females, recognizing them by their pheromones. Up to a hundred males may surround a single female in a “mating ball.” Back in the 1980s, Robert T. Mason and David Crews of the University of Texas discovered that some of the males were producing female-like pheromones. These she-males, as the authors dubbed them, had higher testosterone levels than other males but were not otherwise physically distinctive. Mason and Crews speculated that the female mimics were able to work their way into a better position in the mating ball by confusing other males. Later research suggests that pheromonal mimicry in the garter snake, like the deceptive visual patterns of the cuttlefish, may be a transitory phase rather than a lifelong trait. 

More than any other group of animals, the bony fish have gone in for alternative reproductive strategies in a big way. Parasitic spawning has been documented in 13 fish families. It’s most common among salmonids (salmon and trout), wrasses (tropical reef fish), and cichlids (freshwater fish of African and South American lakes and rivers), but also occurs in blennies, bluegill sunfish, and desert pupfish. 

One of our local piscine celebrities, the plainfin midshipman (Porichthys notatus), perhaps better known as the humming toadfish of Sausalito, has two types of males. Type I males defend territories, vocalize to attract females, fertilize their eggs and defend the clutch until hatching. Type IIs are smaller and non-territorial; their only vocalization is a grunt similar to the female’s. A Type II male hangs around the nest of a Type I until a female enters, then either sneaks in for a quick fertilization or broadcasts his sperm from the nest entrance. Any eggs the Type II manages to fertilize are cared for by the Type I as if they were his own progeny, which makes the Type II a cuckoo-like reproductive parasite. Type II’s invest more than Type I’s in sperm production: a Type II’s testes make up 8.3 percent of its body weight, as opposed to 1.2 percent in Type I’s. 

In coho salmon (Oncorhynchus kisutch), parasitic-spawning males are called jacks. They’re smaller than typical males and spend less time in the ocean before returning to their natal streams. Unlike Type I midshipmen, typical (“hooknose”) male coho will attack these small competitors. At Lagunitas Creek in Marin County, UC Davis fish biologist Peter Moyle watched as a hooknose male “grabbed a jack between its jaws and lifted it out of the water with a shaking motion.” But enough jacks fertilize enough eggs to perpetuate the phenotype. 

Complicated enough for you? A few creatures—crustaceans, fish, reptiles, birds—feature three types of male, each with its own reproductive strategy. More on that next week.