The individuals of many
taxonomic groups of
animals, primarily invertebrates, are hermaphrodites, capable of producing viable gametes of both
sexes. In the great majority of
tunicates,
mollusks, and
earthworms, hermaphroditism is a normal condition, enabling a form of sexual reproduction in which either partner can act as the female or male. Hermaphroditism is
also found in some fish species, but is rare in other
vertebrate groups. Most hermaphroditic species exhibit some degree of self-fertilization. The distribution of self-fertilization rates among animals is similar to that of plants, suggesting that similar pressures are operating to direct the evolution of
selfing in animals and plants.[3]
A rough estimate of the number of hermaphroditic animal species is 65,000, about 5% of all animal species, or 33% excluding insects. Insects are almost exclusively gonochoric, and no definitive cases of hermaphroditism have been demonstrated in this group.[4] There are no known hermaphroditic species among
mammals[5] or
birds.[6]
About 94% of
flowering plant species are either hermaphroditic (all flowers produce both male and female gametes) or
monoecious, where both male and female flowers occur on the same plant. There are also
mixed breeding systems, in both plants and animals, where hermaphrodite individuals coexist with males (called
androdioecy) or with females (called
gynodioecy), or all three exist in the same species (called
trioecy). Sometimes, both male and hermaphrodite flowers occur on the same plant (
andromonoecy) or both female and hermaphrodite flowers occur on the same plant (
gynomonoecy).
Hermaphrodism is not to be confused with
ovotesticular syndrome in mammals, which is a separate and unrelated phenomenon. While people with the condition were previously called "true hermaphrodites" in medical literature, this usage is now considered to be outdated as of 2006 and misleading,[7][8] as people with ovotesticular syndrome do not have functional sets of both male and female organs.[9][10]
Etymology
The term hermaphrodite derives from the
Latin: hermaphroditus, from
Ancient Greek: ἑρμαφρόδιτος,
romanized: hermaphroditos,[11] which derives from
Hermaphroditus (Ἑρμαφρόδιτος), the son of
Hermes and
Aphrodite in
Greek mythology. According to
Ovid, he fused with the
nymphSalmacis resulting in one individual possessing physical traits of male and female sexes.[12] According to the earlier
Diodorus Siculus, he was born with a physical body combining male and female sexes.[13] The word hermaphrodite entered the
English lexicon as early as the late fourteenth century.[14]
Sequential hermaphrodites (
dichogamy) occur in
species in which the individual first develops as one sex, but can later change into the opposite sex.[15] (Definitions differ on whether sequential hermaphroditism encompasses serial hermaphroditism; for authors who exclude serial hermaphroditism, a sequential hermaphrodite is also stipulated to only change sex once.[16]) This contrasts with simultaneous hermaphrodites, in which an individual possesses fully functional male and female genitalia. Sequential hermaphroditism is common in fish (particularly
teleost fish) and many
gastropods (such as the
common slipper shell). Sequential hermaphroditism can best be understood in terms of
behavioral ecology and evolutionary
life history theory, as described in the size-advantage mode[17] first proposed by
Michael T. Ghiselin[18] which states that if an individual of a certain sex could significantly increase its reproductive success after reaching a certain size, it would be to their advantage to switch to that sex.
Sequential hermaphrodites can be divided into three broad categories:
Protandry: Where an organism develops as a male, and then changes sex to a female.[15]
Example: The
clownfish (genus Amphiprion) are colorful reef fish found living in
symbiosis with
sea anemones. Generally one anemone contains a 'harem', consisting of a large female, a smaller reproductive male, and even smaller non-reproductive males. If the female is removed, the reproductive male will change sex and the largest of the non-reproductive males will mature and become reproductive. It has been shown that fishing pressure can change when the switch from male to female occurs, since fishermen usually prefer to catch the larger fish. The populations are generally changing sex at a smaller size, due to
natural selection.
Protogyny: Where the organism develops as a female, and then changes sex to a male.[15]
Example:
Wrasses (Family
Labridae) are a group of reef fish in which protogyny is common. Wrasses also have an uncommon life history strategy, which is termed diandry (literally, two males). In these species, two male morphs exists: an initial phase male and a terminal phase male. Initial phase males do not look like males and spawn in groups with females. They are not territorial. They are, perhaps, female mimics (which is why they are found swimming in group with females). Terminal phase males are territorial and have a distinctively bright coloration.[19] Individuals are born as males or females, but if they are born males, they are not born as terminal phase males. Females and initial phase males can become terminal phase males. Usually, the most dominant female or initial phase male replaces any terminal phase male when those males die or abandon the group.
Bidirectional sex changers: Where an organism has female and male reproductive organs, but may act either as a female or as a male during different stages in life.[15]
Example: Lythrypnus dalli (Family
Lythrypnus) are a group of
coral reef fish in which bidirectional sex change occurs. Once a social hierarchy is established a fish changes sex according to its social status, regardless of the initial sex, based on a simple principle: if the fish expresses subordinate behavior then it changes its sex to female, and if the fish expresses dominant or non-dominant superior behavior then it changes its sex to male.[20]
Dichogamy can have both conservation-related implications for humans, as mentioned above, as well as economic implications. For instance,
groupers are favoured fish for eating in many Asian countries and are often
aquacultured. Since the adults take several years to change from female to male, the
broodstock are extremely valuable individuals.
Pulmonateland snails and land
slugs are perhaps the best-known kinds of simultaneous hermaphrodites, and are the most widespread of terrestrial animals possessing this sexual polymorphism. Sexual material is exchanged between both animals via
spermatophores, and is then stored in the
spermatheca. After exchange of
spermatozoa, both animals will lay fertilized eggs after a period of gestation. The eggs will proceed to hatch after a development period. Snails typically reproduce from early spring through late autumn.[21]
Banana slugs are an example of a hermaphroditic gastropod. Mating with a partner is more desirable biologically than self-fertilization, as the genetic material of the resultant offspring is varied, but if mating with a partner is not possible, self-fertilization is practiced. The male sexual organ of an adult banana slug is quite large in proportion to its size, as well as compared to the female organ. It is possible for banana slugs, while mating, to become stuck together. If a substantial amount of wiggling fails to separate them, the male organ will be bitten off (using the slug's
radula), see
apophallation. If a banana slug has lost its male sexual organ, it can still mate as a female, making hermaphroditism a valuable adaptation.[22]
The species of colourful
sea slugsGoniobranchus reticulatus is hermaphroditic, with both male and female organs active at the same time during copulation. After mating, the external portion of the penis detaches, but is able to regrow within 24 hours.[23][24]
Earthworms are another example of a simultaneous hermaphrodite. Although they possess ovaries and testes, they have a protective mechanism against self-fertilization. Sexual reproduction occurs when two worms meet and exchange
gametes, copulating on damp nights during warm seasons.
The free-living hermaphroditic nematode Caenorhabditis elegans reproduces primarily by self-fertilization, but infrequent out-crossing events occur at a rate of approximately 1%.[25]
Hamlets do not practice self-fertilization, but a pair will mate multiple times over several nights, taking turns between which one acts as the male and which acts as the female.[26][failed verification]
The mangrove killifish (Kryptolebias marmoratus) are simultaneous hermaphrodites, producing both eggs and sperm and routinely reproducing by self-fertilization. Each individual normally fertilizes itself when an egg and sperm produced by an internal organ unite inside the fish's body.[27] This species is also regarded as the only known vertebrate species that can reproduce by
self fertilization.[28]
When
spotted hyenas were first scientifically observed by explorers, they were thought to be hermaphrodites. Early observations of wild spotted hyenas led researchers to believe that all spotted hyenas, male or female, were born with what looked to be a penis. A
female spotted hyena's apparent penis is in fact an enlarged clitoris, which contains an external birth canal.[29][30] It can be difficult to determine the sex of spotted hyenas until
sexual maturity, when they may become pregnant. When a female spotted hyena gives birth, she passes the cub through the cervix internally, but then passes it out through the elongated clitoris.[31]
The term hermaphrodite is used in
botany to describe, for example, a
perfectflower that has both
staminate (male, pollen-producing) and
carpellate (female, ovule-producing) parts. The overwhelming majority of flowering plant species are hermaphroditic.[32]
Monoecy
Flowering plant species with separate, imperfect, male and female flowers on the same individual are called
monoecious. Monoecy only occurs in about 7% of flowering plant species.[33] Monoecious plants are often referred to as hermaphroditic because they produce both male and female gametes. However, the individual flowers are not hermaphroditic if they only produce gametes of one sex.[34] 65% of
gymnosperm species are dioecious, but
conifers are almost all monoecious.[35] Some plants can change their sex throughout their lifetime, a phenomenon called
sequential hermaphroditism.[citation needed]
Andromonoecy
In
andromonoecious species, the plants produce
perfect (hermaphrodite) flowers and separate fertile male flowers that are sterile as female.[36][37] Andromonoecy occurs in about 4000 species of flowering plants (2% of flowering plants).[38]
Gynomonoecy
In
gynomonoecious species, the plants produce hermaphrodite flowers and separate male-sterile pistillate flowers.[36] One example is the meadow saxifrage, Saxifraga granulata.[39] Charles Darwin gave several other examples in his 1877 book "The Different Forms of Flowers on Plants of the Same Species".[40]
About 57% of moss species and 68% of liverworts are
unisexual, meaning that their gametophytes produce either male or female gametes, but not both.[41]: 377
Historically, the term hermaphrodite was used in law to refer to people whose sex was in doubt. The 12th-century Decretum Gratiani states that "Whether an hermaphrodite may witness a testament, depends on which sex prevails" ("Hermafroditus an ad testamentum adhiberi possit, qualitas sexus incalescentis ostendit.").[44][45]
Alexander ab Alexandro (1461–1523) stated, using the term hermaphrodite, that the people who bore the sexes of both man and woman were regarded by the Athenians and the Romans as monsters, and thrown into the sea at Athens and into the Tiber at Rome.[46] Similarly, the 17th-century English jurist and judge
Edward Coke (Lord Coke), wrote in his Institutes of the Lawes of England on laws of succession stating, "Every heire is either a male, a female, or an hermaphrodite, that is both male and female. And an hermaphrodite (which is also called Androgynus) shall be heire, either as male or female, according to that kind of sexe which doth prevaile."[47][48]
During the
Victorian era, medical authors attempted to ascertain whether or not humans could be hermaphrodites, adopting a precise biological definition to the term.[49] From that period until the early 21st century, individuals with
ovotesticular syndrome were termed
true hermaphrodites if their
gonadal tissue contained both testicular and ovarian tissue, and
pseudohermaphrodites if their external appearance (
phenotype) differed from sex expected from internal gonads. This language has fallen out of favor due to misconceptions and stigma associated with the terms,[50][51][8][10] and also a shift to nomenclature based on genetics.
The term "intersex" described a wide variety of combinations of what are ambiguous biological characteristics. Intersex biology may include, for example, ambiguous-looking external genitalia,
karyotypes that include mixed XX and XY chromosome pairs (46XX/46XY, 46XX/47XXY or 45X/XY
mosaic). Clinically, medicine currently uses the terminology "
disorders of sex development" [52] (also known as
variations in sex characteristics.)[53] This is particularly significant because of the relationship between medical terminology and medical intervention.[54]
In some cases, variations in sex characteristics are caused by unusual levels of sex hormones, which may be the result of an atypical set of sex chromosomes.[medical citation needed] One common cause of variations in sex characteristics traits is the crossing over of the
testis-determining factor (SRY) from the Y chromosome to the X chromosome during
meiosis. The SRY is then activated in only certain areas, causing development of
testes in some areas by beginning a series of events starting with the upregulation of the
transcription factor (SOX9), and in other areas not being active (causing the growth of
ovariantissues). Thus,
testicular and ovarian tissues will both be present in the same individual.[57] Though of all total recorded cases of ovotesticular DSD, in only 8% percent of all cases was SRY present, leaving the rest of cases that could be explained to other or less common causes, with the vast majority simply being currently unexplainable.
The evolution of
anisogamy may have contributed to the evolution of simultaneous hermaphroditism and sequential hermaphroditism,[61] it remains unclear if the evolution of anisogamy first led to hermaphroditism or
gonochorism.[62]: 213
A 2023 study argued that hermaphroditism can evolve directly from
mating types under certain circumstances, such as if the fertilization is well organized and the average size of groups is small.[63] Simultaneous hermaphroditism that exclusively reproduces through self-fertilization has evolved many times in plants and animals, but it might not last long evolutionarily.[64]: 14
In animals
Joan Roughgarden and Priya Iyer argued that the last
common ancestor for animals was hermaphroditic and that transitions from hermaphroditism to gonochorism were more numerous than the reverse. Other scientists have criticized this argument; saying it’s based on
paraphyleticSpiralia, assignments of sexual modes for the
phylum level than the species level, and methods exclusively based on
maximum parsimony.[65]
It is widely accepted that the first
vascular plants were outcrossing hermaphrodites.[68] In flowering plants, hermaphroditism is ancestral to dioecy.[69]
Hermaphroditism in plants may promote self fertilization in pioneer populations.[70] However, plants have evolved multiple different mechanisms to avoid self-fertilization in hermaphrodites, including
sequential hermaphroditism, molecular recognition systems and mechanical or morphological mechanisms such as
heterostyly.[71]: 73, 74
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^Schärer L (February 2017).
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^
ab"Is a person who is intersex a hermaphrodite?". Intersex Society of North America. Retrieved 2024-01-20. The mythological term "hermaphrodite" implies that a person is both fully male and fully female. This is a physiologic impossibility. The words "hermaphrodite" and "pseudo-hermaphrodite" are stigmatizing and misleading words.
^
abRosenfield KA (2018), "Hermaphrodite", in Vonk J, Shackelford T (eds.), Encyclopedia of Animal Cognition and Behavior, Cham: Springer International Publishing, pp. 1–2,
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abMills A (2018-01-01).
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ISBN978-1-4875-9337-7. In the past, the term hermaphrodite was widely applied in such cases, but humans are not hermaphroditic. In a truly hermaphroditic species, individuals have functional sets of male and female organs.
^Ghiselin MT (June 1969). "The evolution of hermaphroditism among animals". The Quarterly Review of Biology. 44 (2): 189–208.
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