All male red-sided garter snakes wear female perfume and participate in same-sex copulation every year. (Gender Showcase, 9-12)

Species: Thamnophis sirtalis parietalis

All male garter snakes wear female perfume and participate in same-sex copulation every year.

In 1985 some male garter snakes were found with female perfumes in their skin. Of two hundred mating balls, about 15 percent consisted of a male, presumably with female perfumes in his skin, surrounded by courting males...In choice experiments [tests where they were given a choice between female and feminine male], the males preferred a female to a feminine male, showing that males could tell the difference—they were not deceived.

In 2000 it was found that all male garter snakes have female perfumes when they emerge from the den in the spring and that all males court these perfumed males in addition to females. 

Four Flawed Deceit-Based Hypotheses:

Investigators floated four deceit-based theories to explain why all males have female perfumes on emergence: (1) a perfumed male may confuse the other males while carrying out its own mating; (2) the perfumed male may avoid wasting energy in courting before he has fully awakened from hibernation; (3) a perfumed male may induce the other males to waste time and energy courting him while he gets ready to start his own courting; and (4) a perfumed male may distract other males from females so he has more to himself when he does get going.

The simplest Occam’s Razor hypothesis:

The female perfumes might protect from attack or mounting when he is emerging, to lessen hostility and improve cooperation.

15 percent of garter snake mating balls consist of a male surrounded by courting males.

These snakes appear to participate in group sex every year as a way to improve relationships and reduce aggression.

Photo credit: Flickr user @vabbley

Originally, scientists dismissed this explanation without even considering it, because they thought the theory required that organisms could only be habitually aggressive and antagonistic. Garter snakes tend to be friendly, especially with 20,000 in one giant group sex mating ball!

Citations

• R. Mason and D. Crews, 1985, Female mimicry in garter snakes, Nature 316:59-60

• R. Shine, D. O’Connor, and R. Mason, 2000, Female mimicry in garter snakes: Behavioural tactics of “she-males” and the males that court them, Can. J. Zool. 78-391-96. [Ed. note: Do not use “she-male” to describe transgender people. This is historically used as a harmful pejorative word to demean and exclude.]

• R. Shine, P. Harlow, M. Lemaster, I. Moore, and R. Mason, 2000, The transvestite serpent: Why do garter snakes court (some) other males? Anim. Behav. 59:349-59. [Ed. note: This sensationalist title should not detract from the data recorded or this paper’s role documenting now-revised theories.]See also http://www.naturenorth.com/spring/creatre/garter/Fgarter.html

• Roughgarden, J. (2013) Evolution’s Rainbow: Diversity, Gender, and Sexuality in Nature and People. University of California Press, Berkeley. p. 97-8.

The groove-billed ani bird has 4 types of family structures: 2, 4, 6, & 8 adults. The larger the family, the more protection from predators. (Gender Showcase, 9-12)

Larger groups provide more protection against egg predators.

The ani family shows up in groups of 2 adults (1M1F), 4 adults (2M2F), 6 adults, and 8 adults.

The groove-billed ani (Crotophaga sulcirostris) is an insectivorous black bird with a large, deeply grooved bill. It lives in marshes and open pastures in Central America and is related to the cuckoo. Family organizations of the anis may consist of twosomes with one female and one male, foursomes with two females and two males, sixsomes, and even eightsomes.

An ani foursome is two couples cohabiting a one-bedroom flat with one crib. Nests are built in thorny trees or vines. Each male guards one of the females. A female lays an egg every one to two days. The time from egg-laying to fledgling is three weeks.

Females lay fewer eggs each in 4some than in 2some by laying at different times but stop at same time.

Longer ovulator gets 37% of eggs raised, shorter ovulator gets 63% of eggs raised. Longer ovulator lays larger eggs that hatch earlier w/ better chance of survival.

The two females in a foursome wind up with four eggs total. A female in a twosome can also produce four eggs by herself. Thus the number of eggs laid per female is lower in a foursome than in a twosome.

In a foursome, the females start laying eggs at different times. The starter lays bigger eggs and has a longer time between successive eggs than the follower. Both females stop laying eggs at about the same time. Each female “tosses” out of the nest some of the eggs already laid by the other, with the follower winding up mothering an average 63 percent of the eggs and the starter only 37 percent of the eggs. After the tossing is over, four eggs are left in the nest.

Even though the follower mothers more of the eggs, she doesn’t necessarily successfully raise the most offspring. The starter lays larger eggs, which hatch earlier, so these chicks have a better chance of surviving than chicks from the follower. 

All four birds in a foursome work together to provide for and protect the eggs.

Males divide day into unequal shifts based on oldest getting riskiest shift but also fathers most young.

Photo credit (C) Dave McCauley.

The males divide the day into unequal shifts. The oldest male incubates at night and most of the daylight hours. As a result, he also incurs the most hazard and the highest death rate. Yet he also fathers the most young.

The benefit from predator protection in a larger nesting group outweighs the disadvantages of a crowded family life.

The starter in a foursome produces the most young, a female in a twosome produces an intermediate number of young, and the follower in a foursome the fewest.

Photo credit (C) Joseph Morlan

By why should a female, who can lay four eggs in a twosome without worrying about a nest mate tossing her eggs out, bother living in a foursome? The answer is that the larger group provides protection against egg predators. 

Once loss of eggs to predators is taken into account, the starter in a foursome produces the most young, a female in a twosome produces an intermediate number of young, and the follower in a foursome the fewest. For the anis, the benefit from predator protection of living in extended families of two couples outweighs the disadvantages of a rancorous life at home.

“It’s a cooperative soft goth bird!” —RXS

Citations

• S. Vehrencamp, 1978, The adaptive significance of communal nesting in groove-billed Anis, Behav. Ecol. Sociobiol. 4:1-33.

• B.S. Bowen, R.R. Koford, and S.L. Vehrencamp, Breeding roles and pairing patterns within communal groups of groove-billed Anis, Anim. Behav. 34:347-66.

• Roughgarden, J. (2013) Evolution’s Rainbow: Diversity, Gender, and Sexuality in Nature and People. University of California Press, Berkeley. p. 57-8.

15% of geese pair-bonds are male-male, with some remaining monogamous & cooperative for over 15 years. (Gender Showcase, 9-12)

Scientists have documented same-sex matings in over 94 bird species. One of them is the common goose, Anser anser, who pair-bond for more than a decade and live for 20 years. 

The male goose becomes despondent & defenseless when his same-sex partner dies.

This is the same behavior that between-sex (male-female) goose partners display.

A male is reported to show “grief” after his partner dies, becoming despondent and defenseless, just as between-sex partners do when one dies.

Often one female & 2 males will co-parent a family together.

Geese sometimes form threesomes that are the reverse of oystercatchers: a male pair is joined by a female and the trio raise a family together.

Citations

• F. Cezilly and R.G. Nager, 1995, Comparative evidence for a positive association between divorce and extra-pair paternity in birds, Proc. R. Sox. Lond., ser. B, 262:7-12. 

• T. Clutton-Brock, 1989, Review lecture: Mammalian mating systems, Proc. R. Soc. Lond., ser. B, 236:339-72.

• Roughgarden, J. (2013) Evolution’s Rainbow: Diversity, Gender, and Sexuality in Nature and People. University of California Press, Berkeley. p. 136.

80% of gay swan couples successfully raise their young, compared to 30% of straight swan couples. (Gender Showcase, 9-12)

Life-long pair-bonded male-male couples of the species Cygnus atratus will raise an egg together donated by a female.

Male-male black swan parents are more successful.

80% of gay black swan couples successfully raise their young, but only 30% of straight swan couples successfully raise their young.

Black swans (Cygnus atratus) also form stable male-male pairs that last for many years. Gay swans may even raise offspring together as a couple. A female may temporarily associate with a male-male pair, mate with them, and leave her eggs with them.

By sharing the workload more equally, male-male parents access better nesting sites and territories than straight couples.

The male couple then parents the eggs and is reported to be more successful than a male-female couple because together they access better nesting sites and territories, sharing the workload more equally than between-sex couples.

A full 80-percent of the gay couples successfully fledge their young, compared with 30 percent for straight couples. (EN19)

(EN19) L.W. Braithwaite, 1981, Ecological studies of the black swan: III. Behavior and social organization, Australian Wildlife Research 8:135-46.

Citation: Roughgarden, J. (2013) Evolution’s Rainbow: Diversity, Gender, and Sexuality in Nature and People. University of California Press, Berkeley. p. 136.

Update (5/24/23): Thanks to J. Boeheme at Science TV Australia for clarifying these papers are about black swans, not all swans.

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)

Why do asexual females bother with courtship?

Because they lay twice the number of eggs!

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

1. D. Crews and K. Fitzgerald, 1980, "Sexual" behavior in parthenogenetic lizards (Cnemidophorus), Proc. Nat. Acad. Sci. (USA) 77:499-502

2. D. Crews, 1987, Courtship in unisexual lizards: A model for brain evolution, Scientific American 257 (6): 116-21.

3. 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.

4. 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.

5. C. Cole and C. Townsend, 1983, Sexual behaviour in unisexual lizards, Anim. Behav. 31:724-28.

6. D. Crews and L. Young, 1991, Pseudocopulation in nature in a unisexual whiptail lizard, Anim. Behav. 42:512-14.

7. B. Leuck, 1982, Comparative burrow use and activity patterns of parthenogenetic and bisexual whiptail lizards (Cnemidophorus: Teiidae), Copeia 416-25.

8. B. Leuck, 1985, Comparative social behavior of bisexual and unisexual whiptail lizards (Cnemidophorus), J. Herpetology 19:492-506.

9. Y. Werner, 1980, Apparent homosexual behavior in an all-female population of a lizard, Lepidodactylus lugubris, and its probable interpretation, Tierpsychol. 52:144-50.

10. M.J. McCoid and R.A. Hensley, 1991, Pseudocopulation in Lepidodactylus lugubris, Herpetological Review 22:8-9.

11. 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

12. 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

All female spotted hyenas have penises they use to mount, pee, & give birth. (Gender Showcase, 9-12)

Editor’s note: Earlier, the author defines “penis” in this discussion as something the animal can pee through. —RXS

All female spotted hyenas have functional penises. They use it pee, signal, anally mount males & females for dominance, and give birth.

Intersex plumbing is found in ALL females of the spotted hyena (Crocuta crocuta) of Tanzania—in which the females have penises nearly indistinguishable from those of the males. (EN23)…The first scientific investigation in 1939 showed that a spotted hyena makes only one-size gamete throughout its life, either as an egg or sperm. (EN24) Thus these hyenas are not hermaphrodites. Rather, female spotted hyenas are intersexed, like some female bears.

Editor’s note: The term "hermaphrodite" is appropriate for referring to non-human animals with sex characteristics that do not fit typical binary notions of male or female bodies. For humans, “intersex” is the appropriate term—learn more here!

(EN23) L. Frank, 1996, Female masculinization in the spotted hyena: Endocrinology, behavioral ecology, and evolution, pp. 78-131 in J. Gittleman, ed., Carnivore Behavior and Evolution, vol. 2, Cornell University Press; L. Frank, 1997, Evolution of genital masculinization: Why do female hyenas have such a large ‘penis’? Trends Ecol. Evol. 12:58-62.

(EN24) M. Harrison, 1939, Reproduction in the spotted hyena, Crocuta crocuta (Erxleben.), Phil. Trans. Roy. Soc. Lond., ser. B, 230-1-78.

The females have a phallus 90% as long and the same diameter as a male penis (yes, somebody measured, 171 millimeters long and 22 millimeters in diameter). The labia are fused to form a scrotum containing fat and connective tissue resembling testicles. The urogenital canal runs the length of the clitoris, rather than venting from below. The animal can pee with the organ, making it a penis. Completing the picture, the female penis contains erectile tissue (corpus spongiosum) that allows erections like those of a male penis.

Sex & reproduction with two penises is as costly as pre-Industrial human reproduction, so why has this survived so long? (book excerpt)

A female spotted hyena mates and gives birth through her penile canal. When mating, a female retracts the penis on itself, ‘much like pushing up a shirtsleeve,’ and creates an opening into which the male inserts his own penis. The female’s penis is located in the same spot as the male’s penis, higher on the belly than the vagina in most mammals.

Therefore, the male must slide his rear under the female when mating so that his penis lines up with hers. During birth, the embryo traverses a long and narrow birth canal with a sharp bend in it. About 15% of the females die during their first birth, and they lose over 60% of their firstborn young. (EN 25) These obvious disadvantages lead us to question why female spotted hyenas have this penis instead of a clitoris.

(EN25) L. Frank and S. Glickman, 1994, Giving birth through a penile clitoris: Parturition and dystocia in the spotted hyena (Crocuta crocuta), J. Zoology London 206:525-31; L. Frank, M. Weldele, and S. Glickman, 1995, Masculinization costs in hyenas, Nature 377:584-85.

Erect hyena penises are a sign of submission; the female hyena without the erect penis is the dominant leader of the entire pack. (book excerpt)

Female spotted hyenas have a dominance hierarchy, and the erect penis is a signal of submission. When two females interact with each other in a struggle for dominance, the one who wants to back down signals by erecting her penis. (EN26) No one knows why female hyenas evolved this method of signaling.

(EN26) M. East, H. Hofer, and W. Wickler, 1993, The erect “penis” is a flag of submission in a female-dominated society: Greetings in Serengeti spotted hyenas, Behav. Ecol. Sociobiol. 33:355-70; H. Hofer and M. East, 1995, Virilized sexual genitalia as adaptations of female spotted hyenas, Revue Suisse de Zoologie 102:895-906.

Erections occur in the “meeting ceremony” when animals greet after having been apart. The animals approach each other and stand alongside one another, head-to-tail, one or both lifting her hind leg to allow inspection of her erect penis. When only one member of a greeting pair displays an erection, she is normally the subordinate.

Each hyena puts her reproductive organs next to powerful jaws. Greetings between captive females that have been separated for a week are tense and frequently wind up in a fight that starts when one bites the genitals of the other, doing occasional damage to the reproductive capability of the injured party.

[This] social-inclusionary trait…allows a female hyena access to resources needed for reproduction and survival. If a female were not to participate in social interactions using her penis for signaling, she would not be able to function in hyena society and presumably would either die or fail to breed.

[Testosterone from elevated aggression in hyena society can’t develop] a full-fledged replica of male genital anatomy, complete with scrotal sacs and fat bodies resembling testicles. This structure can’t develop from a few extra splashes of testosterone in the blood.

Citation: Roughgarden, J. (2013) Evolution’s Rainbow: Diversity, Gender, and Sexuality in Nature and People. University of California Press, Berkeley. pp. 138-39.

The sex-changing Australian goby species have 2 sexes: all-female or part-male-part-female. (Gender Showcase, 9-12)

Image credit: Yellowfin Goby, Acanthogobius flavimanus, in Jawbone Marine Sanctuary, Williamstown, Port Phillip, Victoria, February 2018. Source: Wayne Martin / iNaturalist.org. License: CC By Attribution-NonCommercial.

Edit (6/23/21): The book excerpt uses “gender” when it talks about morphology (body plan) in the Barlow study. Thanks to reader Breanna H. for asking about a previous draft of this post that repeated the book’s wording. I learned recently how much K-6 material leans on gender norms to explain biological things. Models are always imperfect, and Breanna refers to a teaching approach that avoids applying the human concept of gender to animals, and a discussion about the risks in conflating sex and gender in animal model studies. (-RXS)

Edit (6/8/23): Thanks to Wayne, adding this: Editor’s note: The term "hermaphrodite" is appropriate for referring to non-human animals with sex characteristics that do not fit typical binary notions of male or female bodies. For humans, “intersex” is the appropriate term—learn more here!(-RXS)

A species of goby from Lizard Island on Australia’s Great Barrier Reef [is the Australian goby].(EN12) In the Australian goby, all the juveniles mature into females, with some later becoming males. The males, however, can change back into females. In fact, the meaning of male is ambiguous here. The investigators defined a male to be any fish with at least some sperm production. All males, however, contain early-stage oocytes—cells that develop into eggs—in their gonads. So all the males remain part female. The species therefore consists of two genders at any one time: all-female fish and part-male-part-female fish.

(EN12 G. Barlow (2000) The Cichlid Fishes: Nature’s Grand Experiment in Evolution. Perseus.)

Citation: Roughgarden, J. (2013) Evolution’s Rainbow: Diversity, Gender, and Sexuality in Nature and People. University of California Press, Berkeley. pp. 137-38.

All bighorn rams that mate with ewes participate in gay courting & copulation most of the year. (Gender Showcase, 9-12)

Bighorn Sheep

1. Males (rams) & females (ewes) live separately except during breeding season.

2. Females are only sexually active 3 days of the year! They refuse all other approaches the rest of the time.

Book excerpt:

The males (rams), with large thick horns that curl back from above the eye to behind the ear, weigh up to 300 pounds. Their macho appearance has become a symbol for many male athletic teams. The females (ewes) live separately from the males. The sexes associate only during the breeding season, called the rutting season, which extends from mid fall to early winter. A female is receptive for about three days, and will not allow herself to be mounted outside of these three days. (EN29)

(EN29 ) V. Geist (1971) Mountain Sheep: A Study in Behavior and Evolution, University of Chicago Press; J.T. Hogg (1984) Mating in bighorn sheep: Multiple creative male strategies, Science 225: 526-29; J.T. Hogg (1987) Intrasexual competition in and mate choice in rocky mountain bighorn sheep, Ethology 75: 119-44.

All male bighorn sheep that breed with female ewes also participate in homosexual courting & anal copulation.

Book excerpt:

The males have been described as “homosexual societies.” Almost all males participate in homosexual courting and copulation. Male-male courtship begins with a stylized approach, followed by genital licking and nuzzling, and often leads to anal intercourse in which one male, usually the larger, rears up on his hind legs and mounts the other. The mounted male arches his back, a posture known as lordosis, which is identical to how a female arches her back during heterosexual mating. The mounting male has an erect penis, makes anal penetration, and performs pelvic thrusts leading to ejaculation.

Source: Roughgarden, J. (2013) Evolution’s Rainbow: Diversity, Gender, and Sexuality in Nature and People. University of California Press, Berkeley. pp. 137-38.

article excerpt:

Four behavioral phenotypes have been described in domestic rams raised in all-male groups: female-oriented, male-oriented, bisexual, and asexual. To make behavioral assignments, rams are first given sexual performance tests, also known as serving capacity tests, to determine whether or not they are attracted to females and to get a measure of their sexual performance.

Source: Roselli, C. E., Reddy, R. C., & Kaufman, K. R. (2011). The development of male-oriented behavior in rams. Frontiers in neuroendocrinology, 32(2), 164–169. https://doi.org/10.1016/j.yfrne.2010.12.007.

Bighorn Sheep have 3 behavior-based genders & 2 body types:

1. Female-body ewes live separately from gay male rams and only accept mounting 3 days of the year.

2. Male-body rams live together separately from females and copulate anally with other male-body sheep most of the year.

3. Male-body rams that live with female-body ewes most of the year and refuse mounting by other male-body rams.

Book excerpt:

The few males who do not participate in homosexual activity…are identical in appearance to other males but behave quite differently. (EN30) They differ from [so-called] “normal males” by living with the ewes rather than joining all-male groups. These males do not dominate females, are less aggressive overall, and adopt a crouched, female urination posture. These males refuse mounting by other males. In physical appearance, including body size and horn development, these males are indistinguishable from other males.

(EN30) J. Berger. (1985) Instances of female-like behaviour in a male ungulate, Anim. Behav. 33:333-35.

Citation: Roughgarden, J. (2013) Evolution’s Rainbow: Diversity, Gender, and Sexuality in Nature and People. University of California Press, Berkeley. pp. 137-38.

Species: Ovis canadiensis (wiki)

Range: North American (Rocky Mountains, Sierra Nevada, southwestern US, Mexico)