All XX Spanish Moles have ovotestes (both ovarian & testicular tissue) and make Eggs & Testosterone, but XY moles only have testes & Make Sperm. (Gender Showcase, 9-12)

Talpa occidentalis (mole, Iberian peninsula)

All females have ovotestes (ovotestes are gonads containing both ovarian & testicular tissue) XX have ovotestes & make eggs and testosterone only, XY have testes only and make sperm only.

Image caption: A Spanish blind mole emerges from underneath a rock. Photo credit (C) Tiago Magalhães.

Most gender-gene committees, with or without the presence of SRY, pass a resolution creating only a testis in males and only an ovary in females. In some species, though, even this most elemental aspect of bodily gender has been given a different configuration.

Among Talpa occidentalis—another burrowing mammal, an old world mole from the Iberian peninsula—all females have ovotestes, gonads containing both ovarian and testicular tissue. The ovotestes occur at the site in the body where simple ovaries are found in other species. 

Talpa XX individuals have ovotestes and make eggs in the ovarian part of their ovotests. They don’t make sperm, but they do have both sperm-related and egg-related ducts. The testicular part of these ovotestes secretes testosterone. XY individuals have testes only and make sperm.

References

  • R. Jiménez, M. Burgos, A. Sánchez, A. Sinclair, F. Alarcón, J. Marin, E. Ortega, and R.D. de la Guardia, 1993, Fertile females of the mole Talpa occidentalis are phynotypic intersexes with ovotestes, Development 118:1303-11.

  • Roughgarden p. 202

The temperature of the nest determines the gonads that form in crocodile eggs. (Gender Showcase, 9-12)

DISCUSSION QUESTIONS:

  1. How do changing temperatures affect a crocodile egg’s development?

  2. How will average global temperature changes affect a crocodile egg’s development?

  3. Predict an increase, decrease, or stable population change if average temperatures increase or decrease.

Book excerpt: Among reptiles, specifically turtles, crocodiles, and some lizards, gonadal identity is determined by the temperature at which eggs develop, not by chromosomes. The eggs are usually laid in the ground and covered with sand or moist dirt from which they absorb water, swelling in size as they age. Reptile embryos start developing within their egg, and after a while primordial germ cells form. When reptile primordial germ cells move to the genital ridges of their parents, both the germ cells and the parental embryo presumably experience the same environmental temperature. Both germ cells and parent therefore receive the same message about which sex to develop as, and their agendas automatically agree.

Scientists reported the first case of intersexuality in an African dwarf crocodile (Osteolaemus tetrapspis), a 10 year-old male-presenting crocodile with gonads that were ovotestes.

We used to think crocodiles couldn’t be intersex, because we had never found any before. Our understand was that crocodiles needed two separate types of cells that never occur together.

This discovery shows we have so many more questions to ask about sex determination!

Image caption: A dwarf crocodile. (C) Jim Frazee

Because the model we use to explain sex determination in crocodiles cannot help explain this evidence, we must keep asking questions and build better models for looking at our evidence.

Langer: Half of the 22 extant species of crocodilians have been examined for occurrence of temperature dependent sex determination (TSD). In TSD reptiles, masculinizing temperatures yield 100% or a majority of males, whereas feminizing temperatures yield 100% or a majority of females. In the transition range of temperature (TRT), a mix of males, females and sometimes intersexes are obtained. However, the molecular mechanisms behind TSD and an explanation for the occurrence of intersexuality remain elusive.

References

  • C. Johnston, M. Barnett, and P. Sharpe, 1995, The molecular biology of temperature-dependent sex determination, Phil. Trans. R. Soc. Lond., ser. B, 350: 297-304.

  • J.W. Lang and H. Andrews, 1994, Temperature-dependent sex determination in crocodilians, J. Exp. Zool. 270-28-44.

  • S. Langer, K. Ternes, D. Widmer, & Frank Mutschmann. The first case of intersexuality in an African dwarf crocodile (Osteolaemus tetraspis). Zoo Biol. 33:459–462, 2014. DOI:10.1002/zoo.21149

  • C. Smith and J. Joss, 1993, Gonadal sex differentiation in Alligator mississippiensis, a species with temperature-dependent sex determination, Cell Tissue Res. 273:149-62. 

  • Wibbles, Bull, and Crews, 1994, Temperature-dependent sex determination. Journal of Experimental Zoology 270(1):71 - 78. DOI: 10.1002/jez.1402700108


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).

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.

Bullfrogs (Rana catesbeiana) have two male genders that both mate with females. (Gender Showcase, 9-12)

Bullfrogs (Rana catesbeiana) have two male genders that both mate with females.

Bullfrogs have two male genders that both mate with females:

(1) large males who call at night, giving bullfrogs their name, and

(2) small males who are silent.

Both are reproductively competent, and females mate with both. Silent males turn into calling males as they grow older. Male frogs in older species and males in many vertebrate groups aslo have to decide when to begin breeding—whether to wait until established enough to flaunt wealth and power, or to begin sooner with fewer resources but lots of charm.

Silent males turn into calling males as they grow older.

Both still mate with females regardless of silence.

Perhaps silent males should not be considered a different gender from calling males, but rather an early developmental stage of the same gender. Compare this case with others, though, and you may agree that it makes more sense to view males who mature from a silent stage into a calling stage as changing genders.

  • R.D. Howard, 1978,. The evolution of mating strategies in bullfrogs, Rana catesbeiana, Evolution 32: 859-71.

  • R.D. Howard, 1981, Sexual dimorphism in bullfrogs, Ecology 62:303-10.

  • R.D. Howard, 1984, Alternative mating behaviors in young male bullfrogs, Amer. Zool. 24:397-406.

  • Roughgarden, J. (2013) Evolution’s Rainbow: Diversity, Gender, and Sexuality in Nature and People. University of California Press, Berkeley. p. 76.

Without sharing food or grooming relationships among all genders, 80% of vampire bats would die from a missed meal instead of 25%. (Gender Showcase, 9-12)

The vampire bat (Demodus rotundus) is a small bat, no bigger than a plum, that “removes a small patch of flesh [from its prey] with its razor-sharp incisors and laps up the blood flowing from the wound. A vampire’s saliva has anticoagulant to keep the blood from clotting. After one bat has drunk its fell, another continues at the same spot.”

Hunting for food is hard and up to one-third of bats miss a meal on any given night.

Bats die after 60 hours without food, after freezing from dropping 25% of its weight.

Life as a vampire is hard. Bats are warm-blooded and, without feathers or fur, lose lots of heat. Their requirements for energy are huge. A vampire bat consumes 50 to 100 percent of its weight in each meal. Yet up to one-third of the bats may not obtain a meal on any given night.

Going without a meal is dangerous. A vampire dies after sixty hours without food because by then its weight has dropped 25 percent, and it can no longer maintain its critical body temperature. To survive, vampire bats have developed an elaborate buddy system for sharing meals. The sharing takes place between mother and pup, as well as between adults.

The dominant male bat fathers half the group’s young by staying and guarding the inner top of the nest.

Subordinate males hang out by the entrance.

Photo credit: Alex Hyde/NPL (https://www.nature.com/articles/d41586-019-03005-5)

One study of vampires on a ranch in Costa Rica focused on a population divided into three groups of a dozen females. The members of a group often stay together for a long time, twelve years in some cases, and get to know one another very well. The group of a dozen adult bats is a family unit from a vampire’s standpoint.

Most of the group consists of females, each of whom usually cares for one pup. A female pup stays in the group as she matures, whereas a male pup leaves. The females in a group span several generations. Group membership is not entirely static, however. A new female joins the group every two years, so at any time the females in the group belong to several lineages, called matrilines.

The bats live in the hollows of trees. Imagine a hollow tree with an opening at its base and a long vertical chamber reaching up into the tree trunk. The females congregate at the top of the chamber. About three males hang out, so to speak, in the tree hollow. 

One male assumes a position near the top of the chamber, nearest to the females, and defends this location against aggressive encounters from other males. This dominant male fathers about half of the group’s young. Subordinate males take up stations near the base of the tree by the entrance. Other males are out of luck, roosting alone or in small male-only groups rarely visited by females.



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70% of food transfers are mother to pup.

The other 30% are female to someone else’s pup, female to female, and male to pup.

Photo credit (C) Gerry Carter

The food is transferred by one bat regurgitating into the mouth of another. Most (70 percent) of the food transfers are from a mother to her pup. This food-sharing supplements the mother’s lactation [milk production]. The other 30 percent involves adult females feeding young other than their own, adult females feeding other adult females, and on rare occasions, adult males feeding offspring.

Increased cooperation in bats includes same-sex grooming and food sharing.

Some adult females have a “special friendship” with females who are not their kin (males also have same-sex relations; see Roughgarden 141). This bond is brought about in part by social grooming. The bats expend 5 percent of each day grooming and licking one another. Some of this grooming is between special friends, and the remaining among kin. A hungry bat grooms one who has recently fed to invite a donation of food. To solicit food, a hungry bat licks a donor on her wing and then licks her lips. The donor may then offer food.

The mutual assistance is significant. If they didn’t help each other, the annual mortality of vampires would be about 80 percent, based on the chance of missing a meal two nights ina row. Instead, the annual mortality rate is around 25 percent because food-sharing tides bats through their bad nights.

References

  • G. Wilkonson, 1990, Food sharing in vampire bats, Scientific American (February), 76-82.

  • Roughgarden uses “cooperation” here in the wider sense to include both helping and not hurting. See R. Trivers, 1984, Social Evolution, Benjamin-Cummings.

  • Roughgarden, J. (2013) Evolution’s Rainbow: Diversity, Gender, and Sexuality in Nature and People. University of California Press, Berkeley. p. 61-2.