Spawning males of the bluegill sunfish have 3 body types/genders of distinct size and color. (Gender Showcase, 9-12)
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).
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.
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.
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.
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.
Many asexually-reproducing Unisexual (all-lesbian) anole lizard species frequently copulate anyway. (Gender Showcase, 9-12)
Confused?
If the entire species is one sex, how can there be lesbian? Doesn’t there have to be something else? Here, “lesbian” is used to refer to how their behavior is based on progesterone cycles but the entire species is one sex; if it were based on testosterone cycles, I assume authors would have referred to it as gay asexual lizards.
If they’re asexual, why are they having sex? Here, “asexual” means they’re able to reproduce without having sex. Some humans identify as asexual, but this is different from the term “asexual reproduction” as it is traditionally used in biology.
Some parthenogenic unisexual species include:
Cnemidophorus inornatus (Arizona whiptail lizard)
Cnemidophorus velox (Colorado whiptail lizard)
Cnemidophorus tesselatus (Colorado whiptail lizard)
Aspidoscelis tesselatus (Common checkered whiptail lizard)
Book Excerpt
Courtship in an asexual species is almost exactly the same [as in sexual species of American whiptail lizards].(EN3) One of the females copies the male role down to the last detail. One mounting female was even seen everting her cloacal region to contact the cloacal area of the mounted female. Courtship between female whiptail lizards is not a sloppy parody of male-female courtship left over from its sexual ancestry, but an intricate and finely honed sexual ritual.
When two females are housed together, they quickly wind up with alternating hormonal cycles. (EN4) As one female cycles into high estradiol, her eggs mature and she assumes the female role in courtship. At the same time, the other cycles into high progesterone (not testosterone) and assumes the male role. Then they switch roles a few weeks later as their hormone cycles switch. (Roughgarden 129)
In nature, asexual females lay an average of 2.3 batches of eggs each season. If a female is housed alone, she lays only about 0.9 batches. If housed with a female whose hormonal state leads to male behavior, she lays 2.6 batches during the season. (Roughgarden 130)
New Mexico’s Environthon reports:
“The New Mexico Whiptail, as well as several other all-female species of whiptail lizard, does reproduce, and all of its offspring are female. Moreover, it reproduces by parthenogenesis -- its eggs require no fertilization, and its offspring are exact and complete genetic duplicates of the mother. Scientists understand only partially how this reproductive mode developed, and it raises many questions. One of the most intriguing is how this cloning affects the lizard's ability to adapt to environmental changes. Since there is no genetic variation except that which occurs through mutation, the New Mexico Whiptail cannot evolve as other species do.”
National Geographic Magazine (Nov 2016 issue) reports on the Baumann team’s research:
“The lizards are all female and parthenogenetic, meaning their eggs develop into embryos without fertilization. But before the eggs form, Baumann’s team discovered, the females’ cells gain twice the usual number of chromosomes—so the eggs get a full chromosome count and genetic variety and breadth (known as heterozygosity) rivaling that of a sexually reproducing lizard.
Why does this occur?
Because long ago, Baumann says, lizards of the genus Aspidoscelis had “a hybridization event”—that is, females of one species broke form and mated with males of another species. Those outlier liaisons gave whiptails robust heterozygosity, which has been preserved by the identical replication—essentially, cloning—that occurs in asexual reproduction. It’s a genetic-diversity advantage that today’s females still enjoy and propagate.”
Crews, D. (1987) Courtship in Unisexual Lizards: A Model for Brain Evolution. Scientific American Vol. 257, No. 6 (December 1987), pp. 116-121. writes:
“The females produce by parthenogenesis, that is, reproduction without fertilization, and therefore copulation between its members is not directly related to the production of offspring. Nevertheless, the females in this species actively engage in courtship rituals that are virtually identical with those observed between male and female whiptail lizards.”
Book Citations: Roughgarden, J. (2013) Evolution’s Rainbow: Diversity, Gender, and Sexuality in Nature and People. University of California Press, Berkeley. pp. 129-131.
Related Citations
D. Crews and K. Fitzgerald, 1980, "Sexual" behavior in parthenogenetic lizards (Cnemidophorus), Proc. Nat. Acad. Sci. (USA) 77:499-502
D. Crews, 1987, Courtship in unisexual lizards: A model for brain evolution, Scientific American 257 (6): 116-21.
L. Young and D. Crews, 1995, Comparative neuroendocrinology of steroid gene expression and regulation: Relationship to physiology and behavior, Trends in Endocrinology and Metabolism 6: 317-23.
D. Crews, M. Grassman, and J. Lindzey, 1986, Behavioral facilitation of reproduction in sexual and unisexual whiptail lizards, Proc. Nat. Acad. Sci. (USA) 83:9547-50.
C. Cole and C. Townsend, 1983, Sexual behaviour in unisexual lizards, Anim. Behav. 31:724-28.
D. Crews and L. Young, 1991, Pseudocopulation in nature in a unisexual whiptail lizard, Anim. Behav. 42:512-14.
B. Leuck, 1982, Comparative burrow use and activity patterns of parthenogenetic and bisexual whiptail lizards (Cnemidophorus: Teiidae), Copeia 416-25.
B. Leuck, 1985, Comparative social behavior of bisexual and unisexual whiptail lizards (Cnemidophorus), J. Herpetology 19:492-506.
Y. Werner, 1980, Apparent homosexual behavior in an all-female population of a lizard, Lepidodactylus lugubris, and its probable interpretation, Tierpsychol. 52:144-50.
M.J. McCoid and R.A. Hensley, 1991, Pseudocopulation in Lepidodactylus lugubris, Herpetological Review 22:8-9.
Dias, B. G., & Crews, D. (2006). Serotonergic modulation of male-like pseudocopulatory behavior in the parthenogenetic whiptail lizard, Cnemidophorus uniparens. Hormones and behavior, 50(3), 401–409. https://doi.org/10.1016/j.yhbeh.2006.05.001
Paulissen, M., & Walker, J. (1989). Pseudocopulation in the Parthenogenetic Whiptail Lizard Cnemidophorus laredoensis (Teiidae). The Southwestern Naturalist, 34(2), 296-298. doi:10.2307/3671747