One sunfish species, the bluegill sunfish (Lepomis macrochirus), has been studied in detail at Lake Opinicon, Ontario, Canada, and at Lake Cazenovia, in upstate New York.
Spawning males consist of three distinct size/color classes, and together with females, fall into four morphological categories, corresponding to four distinct genders:
I think the author, Roughgarden, is using gender to mean that there’s no sexually reproductive distinguishing function, and the difference is strictly morphological and behavioral. This also makes me wonder if the testes are lighter in the small male bluegill sunfish, given that they occupy most of the body cavity but still only comprise 5% of the total body weight of the fish. I am assuming she assigns male and female based on gamete production (egg/sperm) and/or primary regulatory hormone status (progesterone/estrogen/testosterone).
Large male bluegill sunfish are very aggressive, even towards females in their own nest, and defend their nest every 3 minutes.
Females prefer prefer nests with large populations to protect from egg predators.
Image credit: ScienceSource
The yearly spawning episode lasts only one day. In preparation, large males aggressively stake out territories next to one another in aggregations of a hundred or more, called leks, along the bottom of the lake at a depth of 1 meter. Large males are called on to defend their space against neighbors about once every 3 minutes. Large males make nests for eggs in their territories by scooping out a depression in the mud with their tails. Females aggregate at the locales with many males and do not visit isolated or peripheral nests. Females prefer nests belonging to large aggregations because the presence of many males affords more protection from egg predators.
The large males are not Mr. Nice Guys. Their acts of aggression include biting, opercular spreading, lateral displays, tail beating, and chasing. Although primarily directed at intruding males, aggression sometimes is directed at a female in the territory—domestic violence, sunfish style. The male apparently tries to control the speed and timing at which a female lays eggs. Females simply leave if harassed too much in this way.
The females arrive in a school, and one by one they enter the territories of the large males. When a female arrives, a large male begins to swim in tight circles, with the female following. Every few seconds as the pair turns, the female rotates on her side, presses her genital pore against that of the large male, and releases eggs that the large male fertilizes. The egg release is visible as a horizontal dipping motion.
Female bluegill sunfish spawn in many nests that the large, aggressive males guard.
9% of fertilizations are by a neighboring large male who took a break from guarding.
A female may spawn in many nests. A large male accumulates up to thirty thousand eggs from various females during the one-day spawning episode. A female lays about twelve eggs at a time with her dipping motion, so this total egg accumulation involves some female laying in the nest about once every 30 seconds. The scene is fast. Still, large males somehow find the time to enter the nests of neighbors, and about 9% of the fertilizations in a nest are by a neighboring large male.
The more numerous small males quickly fertilize eggs in nests that aren’t their own.
The females only choose nests based on how many fish are around it for protection.
Meanwhile, the small males are active. They stay at the borders between territories of large males and in the periphery, often close to rocks or in vegetation. Eggs remain viable in lake water for about an hour and sperm for only a minute. When the female releases eggs, the small males dart in quickly to release sperm over the eggs and carry out their own fertilizations. The large males try to repel the small males from their territories, but the small males are more numerous than the large males—about 7 to 1 in shallow-water colonies. Chasing all these small males, as well as neighboring large males and the occasional predator, takes a large male away from fertilizing eggs being laid in his territory. In these circumstances, the females spawn readily with small males while the large male is busy with all his chasing.
There are more small males in shallow-water colonies than deep ones because there is more vegetation for cover. It is important to hide because predators—large mouth bass, small-mouth bass, and pike—lurk in the lake. Thus the ratio of small to large males depends on the surrounding environmental context. All in all, the small males seem to be the gender counterpart of silent bullfrogs, silent singing fish, jack and parr salmon, and antlerless male deer.
Medium males: the romantic wingman.
Medium males court with large males, then join them in the nest to mate with a female bluegill sunfish. Both drive away other fish and both mate with the same female.
The medium males—the third male gender—are really surprising. No one knows where the medium males live most of the time, but they may school with the females. A medium male approaches the territory of a large male from above in the water and descends without aggression or hesitation into the large male’s territory. The two males then begin a courtship turning that continues for as long as ten minutes. In the end, the medium male joins the large male, sharing the territory that the large male originally made and defends.
Although the medium male sometimes joins the large male before a female has arrived, more often the medium male joins after a female is already present. The large male makes little if any attempt to drive away the medium male, in contrast to the way the large male drives away small males that dart into the territory.When a female and two males are present, the three of them jointly carry out the courtship turning and mating. Typically, the medium male, who is smaller than the female, is sandwiched between the large male and the female while the [courtship] turning [ritual] takes place. As the female releases eggs, both males fertilize them.
When two females mate with a large male, there is no courtship ritual like between the medium male and the large-male.
The females mate with the large male and then leave without a three-way interaction.
Occasionally, two females may be within a large male’s territory at the same time. Although the large male mates with both females, the three do not participate in any common ritual similar to the three-way interaction of the female with a large and medium male.
After the day’s excitement is over, each large male remains in his territory for 8 to 10 days to guard the eggs. The large male repels nest predators. During this period he never leaves the nest to forage and loses body weight.
% Spawning Groups
In all, 85% of spawning males are either small or medium, with the remaining 15% large males. Although in the minority, large males take part in most of the matings.
Among the large males, the reproductive skew is high and only some of the large males apparently survive the mutual aggression that is necessary to acquire a successful territory. The small and medium males obtain about 14% of the spawnings. Overall, 85% of the territories in which spawning occurs consist of 1 male within 1 female, 11% of 2 or more males and 1 female—usually a large male accompanied by a medium male—and 4% of 1 male and 2 females.
Developmentally, the small and medium males are one genotype, and the large males another. Individuals of the small male genotype transition from the small male gender into the medium male gender as they age, whereas individuals of the large male genotype are not reproductively active until they have attained the size and age fo the large male gender.
Third male as mating facilitator?
Instead of deceit theory or ungendered signaling, Roughgarden proposes a third interpretation:
Once the medium male is sandwiched between the large male and the female during their combined courtship turns, the medium male may protect the female from spawning harassment [from the aggressive large males] through his position between her and the large male.
Also, the medium male may have developed a relationship with the females while schooling with them, and thus able to vouch that the large male is safe.
I suggest that the feminine male is a “marriage broker” who helps initiate mating, and perhaps a “relationship counselor” who facilitates the mating process once the female has entered the larger male’s territory. This service is purchased by the large male from the small male with the currency of access to reproductive opportunity.
Sharing fertilization represents an incentive to stay, not theft...Nothing prevents animals from cooperating in bringing about a mating, as well as in caring for young after a mating...In view of the roles played by the three male genders, let’s agree to call the large male a ‘controller,’ the small male an ‘end-runner,’ and the medium male a ‘cooperator.’
References
For Lake Opinicon studies, see:
M.R. Gross, 1982, Sneakers, satellites and parentals: Polymorphic mating strategies in North American sunfishes, Z. Tierpsychol. 60:1-26.
M. R. Gross, 1991, Evolution of alternative reproductive strategies: Frequency-dependent sexual selection in male bluegill sunfish, Phil. Trans. R. Soc. Lond., ser. B, 332:59-66.
For Lake Cazenovia studies, see:
W.J. Dominey, 1980, Female mimicry in bluegill sunfish—a genetic polymorphism? Nature 284:546–48.
W.J. Dominey, 1981, Maintenance of female mimicry as a reproductive strategy in bluegill sunfish (Lepomis macrochirus), Environ. Biol. Fishes 6:59-64.
Gross, 1991, Evolution of alternative reproductive strategies.
Dominey, 1981, Maintenance of female mimicry as a reproductive strategy in bluegill sunfish.
Roughgarden, J. (2013) Evolution’s Rainbow: Diversity, Gender, and Sexuality in Nature and People. University of California Press, Berkeley. p. 78-81.